Intraoperative Monitoring: Neurophysiology and Surgical Approaches 3030957292, 9783030957292

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Intraoperative Monitoring Neurophysiology and Surgical Approaches Silvia Mazzali Verst Maria Rufina Barros Marcos Vinicius Calfat Maldaun Editors

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Intraoperative Monitoring

Silvia Mazzali Verst Maria Rufina Barros Marcos Vinicius Calfat Maldaun Editors

Intraoperative Monitoring Neurophysiology and Surgical Approaches

Editors Silvia Mazzali Verst Instituto de Ensino e Pesquisa (Research and Teaching Institute) Hospital Sírio Libanês São Paulo, Brazil

Maria Rufina Barros Neurophisiology Department Vitoria Apart Hospital Serra, Espírito Santo, Brazil

Marcos Vinicius Calfat Maldaun Neurosurgery Department Hospital Sírio Libanês São Paulo, São Paulo, Brazil

ISBN 978-3-030-95729-2    ISBN 978-3-030-95730-8 (eBook) https://doi.org/10.1007/978-3-030-95730-8 © The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 This work is subject to copyright. All rights are solely and exclusively licensed by the Publisher, whether the whole or part of the material is concerned, specifically the rights of reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, expressed or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. This Springer imprint is published by the registered company Springer Nature Switzerland AG The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland

From Silvia: To my husband Heinz and our children Thomas and Lisa, for enabling me to fly high. From Rufina: To Jefferson (in memoriam), my beloved husband, best friend, and supporter, who rose to other dimensions during this project, and to Catarina, our daughter. “We are what we repeatedly do; excellence, then, is not an act but a habit.” Aristotle

Foreword

This book is the culmination of all the collective shared experiences of the authors. When the idea of writing this book came about, it was because of a desire to share our knowledge and experience that we have gained over the many years in performing intraoperative neurophysiologic monitoring (IONM). Some of us, including my good friend and compadre Dr. Ricardo Ferreira and I, were self-taught and learned how to conduct IONM essentially “on the job.” Of course, we had the proper clinical neurophysiology foundation to be able to build on, but we “learned” IONM because we found the field fascinating and understood that we could have a direct and profound impact on patient care during surgery. Not having been previously exposed to IONM, once I did my first case in 1993, I realized that there is another world of clinical neurophysiology where it can be applied in a very dynamic fashion and where our clinical neurophysiologist’s decisions can have immediate impact on the patient’s surgical outcome. We realized that we could prevent neurologic injury, including stroke, spinal cord, and peripheral nerve injury among others. We could also guide and alter surgical management. All these things were completely new and addictive to those of us who started before there were any formal training programs in IONM. An important point to make is that all the contributors are individuals who actually “do” IONM. By that I mean they know how to setup cases, place electrodes on patients, run the IONM equipment, and troubleshoot technical problems, and they are available throughout the patients’ operative procedure. That’s the way we train our IONM fellows at Stanford. Many of the authors, especially those in South American countries, take it a step further and run their cases from beginning to end without help from technologists. Thus, it has been our desire and drive to teach and pass the knowledge and experience that we have gained “the hard way” to those now coming into the field. This book helps to serve that purpose. Here is our collective knowledge and experience gained over many years, from thousands of cases; from research, conferences, collaborative work, and recommendations; and from colleagues’ advice. Our intent is to present IONM in a comprehensive but concise and practical manner so that all practitioners in the field will find it useful and can take the information and apply it to their patients. vii

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Foreword

The inspiration and impetus for creating this book come from many; however, the heart and driving forces behind this come from Rufina Barros and Silvia Verst. Without them, this collective work, which took 2 years to complete, would not have materialized. Recruiting authors, coaxing them to write their chapters, and trying to adhere to a deadline, all of which occurred while they still had to fulfill their IONM clinical duties in the middle of a global pandemic, were truely colossal efforts. I hope that the contents of this book become a practical reference in the comprehensive education of IONM and can form a foundation for those starting in the field. My ultimate desire is that all who read this book get a chance to monitor a case covered in each chapter and that for every novel case you monitor, you contact the author of the chapter that it corresponds. Stanford, CA, USA August 20, 2021

Jaime R. López

Preface

The completion of this project has been quite a challenge since it was undertaken during a pandemic that affected most of the authors. Many lost their loved ones and suffered under personal and familiar illnesses. We cannot sufficiently express our thankfulness to those who managed to complete their chapters. This book started with the desire to share the experience and expertise of neurophysiologists who deal with many difficulties in the operating room during their daily practice and yet manage to hold on to high standards of care. IOM quality relies in technical details that must not be overlooked. As Rufina says, “the frog jumps out due to necessity.” The frog in this case is the neurophysiologist overcoming economic and scientific barriers present in underdeveloped countries. It includes travelling abroad to refine technical knowledge and buying intraoperative systems at their own expense. It goes further by not having the possibility of using expensive and specially designed electrodes. Despite that, the neurophysiologist can perform the “proper jump.” Aage Moller told Rufina in Croatia in 2009 that “neurosurgeons started intraoperative neurophysiology monitoring, but it is up to neurophysiologists to bring it a step forward.” It has become true in many ways. Innovations are occurring quickly, leading to refinements in many techniques, like in motor-evoked potentials, awake craniotomies, and peripheral nerves approach, to name a few. Innovations start anywhere in the world, and we could successfully add some to the book. Many of the authors are global pioneers in IOM since they debuted at a time when not even motor-evoked potentials were available in the operating room. Since then, accumulated development has resulted in renowned books on this subject. It was challenging to develop a project that equalized with those. This book does not aim to exhaust the subject of IOM but to contribute to the field. We have been engaged in educational projects and activities over the years. We simply love teaching because it enables us to translate complex subjects into easily understandable content. Besides that, we are directly engaged in fellowship programs for neurosurgeons in neuro-oncology (Maldaun) and neurophysiologists in intraoperative monitoring (Verst), aiming to fill a gap and share our experience in

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the field. Training is a difficult task, but it is rewarding if you achieve to inspire others to strive for high quality in healthcare. We were able to manage this project because of our long trajectory in the search for excellence. It was a life’s choice since it held us apart from familiar and social living. Thus, it is paramount to thank the most important people: • To our families whose selflessness has allowed us to spend a large part of our lives in the pursuit of knowledge. It would not have been possible without their love, understanding, and partnership. • To our patients who trusted their lives in our hands. • To the surgeons who see us as a fundamental member of the teamwork. • To our medical associates, technicians, and fellows, whose daily conviviality gives us support, responsibilities, and focus. We would like to individually name everyone who supported our project, but that is not feasible. Yet, there are some that we cannot miss because of their great help at critical moments. Our special thanks to Ricardo Ferreira who encouraged and helped many authors during their writing and took over many chapters on his own, as well as to • Partha Thirumalla, who believed and jumped into this project since the very beginning • Kathleen Seidel, whose care and kindness was a refreshment along the way • Linda Wilson-Pauwells, João Tiago Alves, and Luana Bulgarelli, whose incredible illustrations enrich many chapters • The Springer staff, who helped us throughout the editorial process São Paulo, SP, Brazil Serra, ES, Brazil São Paulo, SP, Brazil

Silvia Mazzali Verst Maria Rufina Barros Marcos Vinicius Calfat Maldaun

Contents

Part I Overview 1 History of Intraoperative Neurophysiological Monitoring in Brazil: Reports from the Pioneers and a Glance in Latin America��������������������������������������������������������������������������������������    3 Andreya Fonseca Cardoso Cavalcanti and Francisco Soto 2 Intraoperative Neurophysiological Monitoring in Brazil: Regulatory Aspects, Training, and Evidence Level������������������������������   39 Carlo Domênico Marrone and Andréa Broisler Sucena Caivano 3 Muscle Motor Point Atlas and Needling Pitfalls ����������������������������������   57 Bruno Nogueira da Silva and Tae Mo Chung 4 Safety and Troubleshooting��������������������������������������������������������������������   89 Jose Alberto Nunes Sobrinho, Monica Nascimento de Melo, and Silvia Mazzali Verst 5 Central Nervous System Anesthesia: Asleep Approach������������������������  111 Nelson Mizumoto Part II Neurophysiological Modalities Applied to IOM 6 Brainstem Auditory Evoked Potentials��������������������������������������������������  129 Jamison Beiriger, Varun Shandal, Josh Sunderlin, and Parthasarathy D. Thirumala 7 Evoked Potential – Visual Pathways Approach beyond Visual Evoked Potentials ������������������������������������������������������������������������  143 Monica Nascimento de Melo and Silvia Mazzali Verst 8 Somatosensory Evoked Potentials����������������������������������������������������������  165 Jamison Beiriger, Varun Shandal, Josh Sunderlin, and Parthasarathy D. Thirumala

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9 Motor Evoked Potential��������������������������������������������������������������������������  181 Carla Ferreira and Silvia Mazzali Verst 10 Intraoperative Monitoring: Electroencephalogram ����������������������������  203 Maria Lucia Furtado de Mendonça and Francisco José Carchedi Luccas 11 Electromyography������������������������������������������������������������������������������������  225 Francisco Tellechea Rotta, Carlo Domênico Marrone, and Ana Maria Hoppe 12 Brainstem Reflexes����������������������������������������������������������������������������������  237 Isabel Fernández-Conejero and Sedat Ulkatan Part III Brain Functions: Eloquent Areas 13 The Brain Surface������������������������������������������������������������������������������������  253 Eduardo Carvalhal Ribas and Guilherme Carvalhal Ribas 14 Brain Functions: Eloquent Areas – Motor and Somatosensory����������  269 Kathleen Seidel and Marcos Vinicius Calfat Maldaun 15 Anesthesia: Awake Approach������������������������������������������������������������������  287 Vinicius Gonçalves Vieira 16 Anatomy: Language Network and DTI ������������������������������������������������  301 João Tiago Alves-Belo 17 Awake Surgery: Performing an Awake Craniotomy����������������������������  327 Silvia Mazzali Verst, Juliana Ohy, Cleiton Formentin, and Marcos Vinicius Calfat Maldaun 18 Language and Cognitive Tests: A Target-­Guided Protocol������������������  357 Silvia Mazzali Verst, Tatiana Vilasboas Alves, and Leonardo Dornas de Oliveira Part IV Brainstem and Cranial Nerve Function 19 Cranial Nerve Monitoring III to XII������������������������������������������������������  387 Silvia Mazzali Verst, Maria Rufina Barros, and Rayssa Addiny Modenesi Lozano 20 Fourth Ventricle’s Floor Mapping����������������������������������������������������������  421 Kathleen Seidel and Andreas Raabe 21 Microvascular Decompression����������������������������������������������������������������  431 Jamison Beiriger, Varun Shandal, Josh Sunderlin, and Parthasarathy D. Thirumala

Contents

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Part V Spine and Spinal Cord Surgery 22 Spinal Deformity Surgery ����������������������������������������������������������������������  459 Ricardo José Rodriguez Ferreira, Emília Caram Bordini, André Cleriston J. dos Santos, Roberto Waldesmand Farias Pontes, Paulo Tadeu Maia Cavali, and Tiago Bertacini Gonzaga 23 Lumbar Interbody Fusion Surgeries: LIFS������������������������������������������  495 Ricardo José Rodriguez Ferreira, Marcus Vinícius Magno Gonçalves, Emília Caram Bordini, and Alexandre Fogaça Cristante 24 Cervical Spinal Surgery��������������������������������������������������������������������������  513 Ricardo José Rodriguez Ferreira, Patrícia Toscano, Emília Caram Bordini, and Arthur Werner Poetscher 25 Tethered Cord Syndrome������������������������������������������������������������������������  539 Vanise Campos Gomes Amaral, Sérgio Cavalheiro, Ricardo José Rodriguez Ferreira, and Maria Lucia Furtado de Mendonça 26 Selective Dorsal Rhizotomy and Intraoperative Neurophysiological Monitoring: Theory to Practice����������������������������  565 Carlo Domênico Marrone, André Bedin, Ana Maria Hoppe, Cristiane Soveral D’Aviz, and Jorge Wladimir Junqueira Bizzi 27 Intramedullary Spinal Cord Tumors ����������������������������������������������������  587 Andreya Fonseca Cardoso Cavalcanti, Karina Maria Alécio de Oliveira, Monica Nascimento de Melo, and Silvia Mazzali Verst Part VI Vascular Surgery 28 Intraoperative Neurophysiologic Monitoring of Cerebrovascular Disorders��������������������������������������������������������������������������������������������������  611 Jaime R. López and Felix W. Chang 29 Intraoperative Neurophysiologic Monitoring for Thoracic and Thoracoabdominal Aortic Procedures��������������������������������������������  661 Felix W. Chang and Jaime R. López Part VII Pheripheral Nerve Surgery 30 Peripheral Nerve: Neurophysiology as a Tool to Optimize Topographic Accuracy and Surgical Planning��������������������������������������  711 Maria Rufina Barros

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Part VIII Head and Neck Surgery 31 Monitoring in Facial, Neck, and Ear Surgeries������������������������������������  745 Karina Maria Alécio de Oliveira, Estela Lladó-Carbó, Ricardo José Rodriguez Ferreira, Marcus Vinícius Magno Gonçalves, and Marina Azzi Quintanilha Part IX Epilepsy Surgery 32 Intraoperative Monitoring in Epilepsy Surgery ����������������������������������  781 Vera Cristina Terra, Marcelo Volpon, and Hélio Rubens Machado Part X Movement Disorders Surgery 33 Neurophysiological Guidance for Movement Disorder Surgery ��������  817 Denise Spinola Pinheiro and Erich Fonoff Part XI Special Topics 34 IOM in Pelvic Floor: Gynecological and Urological Surgeries������������  839 Ricardo José Rodriguez Ferreira, Emília Caram Bordini, Guillermo Martín-­Palomeque, Lidia Cabañes-Martinez, and Nucelio Luiz De Barros Moreira Lemos Index������������������������������������������������������������������������������������������������������������������  865

Contributors

Tatiana  Vilasboas  Alves  Neurosurgeon at São Camilo Hospital, Unit Pompéia, São Paulo, Brazil João Tiago Alves-Belo  Neurosurgery Department, Hospital Felício Rocho, Belo Horizonte, MG, Brazil Vanise  Campos  Gomes  Amaral  Universidade do Estado do Amazonas/Escola Superior de Ciências da Saúde-UEA/ESA, Manaus, AM, Brazil Maria  Rufina  Barros  Department of Intraoperative Monitoring, Neurological Institute of Espirito Santo, Vitória, ES, Brazil Department of Neurophysiology, Vitoria Apart Hospital (VAH), Vitória, ES, Brazil André Bedin  Brazilian Society of Pediatric Surgery, Porto Alegre, RS, Brazil Jamison Beiriger  School of Medicine, Drexel University, Philadelphia, PA, USA Jorge  Wladimir  Junqueira  Bizzi  Pediatric Neurosurgery Department, Clinical Hospital of the Medical School of the University of Rio Grande do Sul, Porto Alegre, RS, Brazil Emília  Caram  Bordini  AACD - Disabled Child Care Association, São Paulo, SP, Brazil Dr Ricardo Ferreira Clinic, São Paulo, SP, Brazil Spine Surgery Department at Orthopedics and Trauma Institute of Clinical Hospital of the University of São Paulo Medical School, São Paulo, SP, Brazil Lidia  Cabañes-Martinez  Clinical Neurophysiology, Hospital Ramón y Cajal, Madrid, Spain Andréa  Broisler  Sucena  Caivano  Biomedical Technologist, Brain Spine Neurofisiologia, São Paulo, São Paulo, SP, Brazil Andreya  Fonseca  Cardoso  Cavalcanti  Department of Neurology Neurophysiology, Neurocol Neurofisiologia Avançada, São Paulo, SP, Brazil

and

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Sérgio  Cavalheiro  Department of Neurosurgery, Universidade Federal de São Paulo, São Paulo, SP, Brazil Paulo  Tadeu  Maia  Cavali  Scoliosis Group, AACD - Disabled Child Care, Association, São Paulo, SP, Brazil Scoliosis Department at Sirio Libanês Hospital, São Paulo, SP, Brazil Felix  W.  Chang  Department of Neurology and Neurological Sciences, Stanford University, Stanford, CA, USA Tae  Mo  Chung  Clinical Neurophysiology Coordinator, Physical Medicine and Rehabilitation Department at the Clinical Hospital of University of São Paulo Medical School, São Paulo, SP, Brazil Alexandre  Fogaça  Cristante  Spine Surgery Department at Orthopedics and Trauma Institute of Clinical Hospital of the University of São Paulo Medical School, São Paulo, SP, Brazil Cristiane  Soveral  D’Aviz  Department of Neurophysiology – Santa Casa de Misericórdia de Porto Alegre/RS, Porto Alegre, RS, Brazil Isabel Fernández-Conejero  University Hospital of Bellvitge, Barcelona, Spain Ricardo  José  Rodriguez  Ferreira  AACD - Disabled Child Care Association, São Paulo, SP, Brazil Dr Ricardo Ferreira Clinic, São Paulo, SP, Brazil Spine Surgery Department at Orthopedics and Trauma Institute of Clinical Hospital of the University of São Paulo Medical School, São Paulo, SP, Brazil Carla Ferreira  Clinical Hospital of the Federal University of Minas Gerais, Belo Horizonte, MG, Brazil Erich  Fonoff  Department of Neurology, University of São Paulo, São Paulo, SP, Brazil Cleiton  Formentin  Researcher at Instituto de Ensino e Pesquisa (Teaching and Research Institute) of Hospital Sirio Libanês, São Paulo, SP, Brazil Marcus  Vinícius  Magno  Gonçalves  Neurologist and Neurophysiologist, Neurology at the University of the Region of Joinville (UNIVILLE), Joinville, Brazil Tiago  Bertacini  Gonzaga  Anesthesiology Department, AACD - Child Care Association, São Paulo, SP, Brazil Ana Maria Hoppe  Department of Neurophysiology, Santa Casa de Misericórdia de Porto Alegre, Porto Alegre, RS, Brazil Nucelio Luiz De Barros Moreira Lemos  Gynecology Department, University of Toronto, Toronto, ON, Canada

Contributors

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Estela  Lladó-Carbó  Clinical Neurophysiology Department, Neurotoc Intraoperative Neuromonitoring company- (Spain), HM Catalunya Hospital, Barcelona, Spain Jaime R. López  Department of Neurology and Neurological Sciences, Stanford University, Stanford, CA, USA Department of Neurosurgery (Courtesy), Stanford University, Stanford, CA, USA Rayssa  Addiny  Modenesi  Lozano  Clinical Neurophysiologist at Brain Spine Neurofisiologia, São Paulo, Brazil Francisco José Carchedi Luccas  Clinical Neurophysiology, Hospital São Luiz – Morumbi – Rede D’Or, São Paulo, SP, Brazil Hélio Rubens Machado  Center for Epilepsy Surgery, Department of Surgery and Anatomy, Ribeirao Preto Medical School, University of Sao Paulo, Ribeirao Preto, Sao Paulo, Brazil Marcos Vinicius Calfat Maldaun  Instituto de Ensino e Pesquisa (Teaching and Research Institute) of Hospital Sirio Libanês, São Paulo, SP, Brazil Neurosurgery Department, Hospital Sirio Libanês, São Paulo, São Paulo, Brazil Carlo  Domênico  Marrone  Past President of the Brazilian Clinical Neurophysiology Society, Porto Alegre, RS, Brazil Intraoperative Neurophysiological Monitoring, Department Coordinator of Hospital da Criança Santo Antônio, Porto Alegre, RS, Brazil Universidade Federal de Ciências da Saúde de Porto Alegre - UFCSPA, Porto Alegre, RS, Brazil Clínica Marrone, Clinical Neurophysiology, Porto Alegre, RS, Brazil Guillermo  Martín-Palomeque  Clinical Neurophysiology, Hospital Ramón y Cajal, Madrid, Spain Silvia  Mazzali  Verst  Instituto de Ensino e Pesquisa (Research and Educational Institute) of Sírio Libanês Hospital, São Paulo, Brazil Brain Spine Neurofisiologia, Jundiaí, SP, Brazil Monica  Nascimento  de Melo  Department of Neurophysiology, Integrated Neuroscience Institute, Goiânia, GO, Brazil Maria  Lucia  Furtado  de Mendonça  Clinical Neurology and Neurophysiology, Intraoperative and Critical Care Clinical Neurophysiology, Neuro Logical Clinica Médica, Rio de Janeiro, RJ, Brazil Nelson Mizumoto  Anesthesiology Coordinator at the Neurosurgery Department, Clinical Hospital of University of Sao Paulo Medical School, Sao Paulo, Brazil

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Juliana Ohy  Researcher at Instituto de Ensino e Pesquisa (Teaching and Research Institute) of Hospital Sirio Libanês, São Paulo, SP, Brazil Leonardo Dornas de Oliveira  Hospital das Clínicas da Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil Karina Maria Alécio de Oliveira  Department of Neurology and Neurophysiology, Clinica Stela de Monitoramento Clínico e Cirúrgico em Neurologia, Brasília, DF, Brazil Denise Spinola Pinheiro  Department of Neurology, Universidade Federal de São Paulo, São Paulo, SP, Brazil Arthur Werner Poetscher  Neurosurgery Department at Hospital Israelita Albert Einstein, São Paulo, SP, Brazil Roberto  Waldesmand  Farias  Pontes  Neurology and Neurophysiology Department, Ribeirão Preto Medical School of the, University of São Paulo, Ribeirão Preto, SP, Brazil Marina Azzi Quintanilha  Cervical and Head Surgery Department, CICAP, Centro Clínico Sudoeste, Brasília, DF, Brazil Andreas  Raabe  Department of Neurosurgery, Inselspital, Bern University Hospital, University of Bern, Bern, Switzerland Eduardo Carvalhal Ribas  Hospital Israelita Albert Einstein, São Paulo, SP, Brazil University of São Paulo Medical School, São Paulo, SP, Brazil Guilherme  Carvalhal  Ribas  Hospital Israelita Albert Einstein, São Paulo, SP, Brazil University of São Paulo Medical School, São Paulo, SP, Brazil Francisco Tellechea Rotta  Intercoastal Medical Group, Sarasota, FL, USA André  Cleriston  J.  dos Santos  Neurology and Neurophysiology Department, Ribeirão Preto Medical School of the, University of São Paulo, Ribeirão Preto, SP, Brazil Kathleen  Seidel  Department of Neurosurgery, Inselspital, Bern University Hospital, University of Bern, Bern, Switzerland Varun  Shandal  Department of Neurological Surgery, Center for Clinical Neurophysiology, University of Pittsburgh, Pittsburgh, PA, USA Bruno  Nogueira  da Silva  Clinical Neurophysiologist by Brain Spine Neurofisiologia, Jundiai, SP, Brazil Jose  Alberto  Nunes  Sobrinho  Department of Neurophysiology, Stela Clinic, Brasilia, Brazil

Contributors

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Francisco Soto  Department of Neurology, Las Condes Clinic, Santiago, Chile Josh  Sunderlin  Procirca, Clinical Neurophysiology, University of Pittsburgh Medical Center, Pittsburgh, PA, USA Vera Cristina Terra  Centro de atendimento Integral das Epilepsias, Nossa Senhora das Graças Hospital, Rua Alcides Munhoz, Curitiba – PR, Brazil Parthasarathy  D.  Thirumala  Department of Neurological Surgery, Center for Clinical Neurophysiology, University of Pittsburgh, Pittsburgh, PA, USA Department of Neurology, University of Pittsburgh, Pittsburgh, PA, USA Department of Neurological Surgery and Neurology, University of Pittsburgh, Pittsburgh, PA, USA Patrícia  Toscano  Neurology Department, Ribeirão Preto Medical School of the University of São Paulo, Ribeirão Preto, SP, Brazil Sedat Ulkatan  Mount Sinai West Hospital, New York, NY, USA Vinicius  Gonçalves  Vieira  Anesthesiology Department, Sírio Libanês Hospital, São Paulo, SP, Brazil Marcelo  Volpon  Center for Epilepsy Surgery & Department of Surgery and Anatomy, Ribeirão Preto Medical School of the University of São Paulo, Ribeirão Preto, SP, Brazil

Part I

Overview

Chapter 1

History of Intraoperative Neurophysiological Monitoring in Brazil: Reports from the Pioneers and a Glance in Latin America Andreya Fonseca Cardoso Cavalcanti and Francisco Soto

Introduction Writing history is complex and has inaccuracies and biases as it can depend on the author’s point of view. Therefore, it is understandable that there are different versions of the same period of history. However, there is only one truth and it is essential to recognize that it is often not possible to fully know it. Over the past 40 years, intraoperative neurophysiological monitoring (IOM) has grown from an investigational procedure into a widely used method, aiming to protect patients from neurologic injury during surgery. However, it was only more recently, in the last 20 years, with the introduction and popularization of the use of motor evoked potential (MEP) in the operating room (OR), that the evaluation of motor pathways boosted the spread of IOM around the world. Companies invested in equipment and production of supplies to this emerging medical field. IOM clinical papers popped up and departments were structured in Universities Medical Centers. Despite or due to the great growth of knowledge in IOM, the number of properly trained and qualified professionals is still far below the world demand. And Brazil is no exception. Latin America had a creative, early, and robust development in this area of clinical neurophysiology, which was recognized worldwide by different international societies that approached the continent to participate and foster this development.

A. F. C. Cavalcanti (*) Department of Neurology and Neurophysiology, Neurocol Neurofisiologia Avançada, São Paulo, SP, Brazil e-mail: [email protected] F. Soto Department of Neurology, Las Condes Clinic, Santiago, Chile © The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 S. M. Verst et al. (eds.), Intraoperative Monitoring, https://doi.org/10.1007/978-3-030-95730-8_1

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A. F. C. Cavalcanti and F. Soto

This achievement was based on the hard and consistent work of a few Latin American neurophysiologists, initially scarce, but many more were added over time. To systematize the global, Latin American, and Brazilian context of the IOM, the chapter is subdivided into three large sections: 1. Timeline of IOM Evolution in the World 2. Overview of IOM History in Latin America

2.1 Origins of IOM in Latin America 2.2 Influence of International Mentors and Societies 2.3 Special Interest Group in IOM and Latin American IOM Events 2.4 Congress and Course of the International Society of Intraoperative Neurophysiology (ISIN) Rio 2015

3. History of IOM in Brazil

3.1 Overview of the Late 1980s and Early 1990s 3.2 Experience and Reports of the Brazilian Pioneers 3.3 Academic Training in IOM in Brazil 3.4 Evolution of IOM Equipment and Its Arrival in Brazil 3.5 Brazilian Society of Clinical Neurophysiology (SBNC)



3.5.1 IOM Events by SBNC 3.5.2 Development of IOM Department at SBNC



3.6 Current Status of IOM in Brazil and Latin America

Timeline of IOM Evolution in the World • 1898: Fedor Krause stimulated the facial nerve to observe its functioning [1]. • 1937: Penfield used direct cortical stimulation to define the homunculus of human motor and sensory cortex [2]. • 1949: Electrocorticography (ECoG) was used to identify regions of epileptic discharges [3, 4]. • 1959: Penfield & Robert: First language mapping during awake craniotomy [5]. • Late 1960s and early 1970s: Electroencephalogram (EEG) was carried out in carotid endarterectomy [6–8]. • Early 1970s: Ojeman proposed a methodology for language mapping during awake craniotomy [9]. Directly recorded spinal potentials from the epidural space after direct spinal stimulation [10–13]. • 1974: Middle- and long-latency somatosensory evoked cortical potentials (SEP) started to be applied in the OR [14]. • 1977: Nash in the USA and Tamaki in Japan started monitoring spinal deformities in young children [15, 16]. • Late 1970s and early 1980s: Technical improvements on SEP, which became a widely adopted method of spinal cord monitoring [17].

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• Early 1980s: IOM began to be mentioned in academic meetings [18]. • 1981: Commercial IOM equipment became available [18]. • 1985: Use of auditory evoked potentials and electroneuromyography during surgery around cranial nerves [19, 20]. • Mid-1980s: IOM-specific meetings began to be offered [18]. • 1986: The first IOM textbook (Nuwer) was published [18]. • 1988: The second IOM textbook (Moller) was released [18]. • Late 1980s: IOM became an established technique widely used. • 1991: Hicks and Burke described the use of transcranial electrical stimulation with epidural recording as a corticospinal evaluation technique for use under anesthesia [21, 22]. • 1993: Taniguchi described the technique of transcranial electrical stimulation with muscle registration for use under anesthesia: Popularization of MEP in the OR [23]. • 1998: Deletis, Kothbauer, and Epstein implemented transcranial electrical single pulse stimulation with D wave spinal cord recording with multipulse transcranial stimulation with myogenic recording in intramedullary spinal cord tumors [24]. • 2002: Food and Drug Administration (FDA) approval of the first commercially available transcranial electrical stimulator (Digitimer D185) [25].

Overview of IOM History in Latin America Origins of IOM in Latin America In 1994, the Head of the Department of Neurosurgery at the Las Condes Clinic (Santiago, Chile), the prestigious neurosurgeon Professor Luciano Basauri, MD, contacted the neurologist Francisco Soto, MD, to give him a mission: to develop intraoperative neurophysiological monitoring in complex surgeries of the Central and Peripheral Nervous System. There was nothing similar in Chile. Basauri recommended Soto to a personal friend at New York University (NYU), Fred Epstein, MD (†). Epstein was a world famous and charismatic neurosurgeon. His skill was to operate inoperable Central Nervous System tumors, especially intramedullary tumors. In 1996, the NYU Department of Neurosurgery organized a course, not knowing that the first steps were being taken to found intraoperative monitoring in Latin America. In this course, the enthusiastic Professor Epstein stated bluntly: “Intraoperative neurophysiological monitoring constitutes the greatest revolution in neurosurgery at the end of the 20th century”. The secret that Epstein kept for the resection of inoperable tumors with the least possible neurological deficit was the intraoperative neurophysiology. Epstein generously shared that he used it in all his surgeries. It was implemented by Vedran Deletis, MD, PhD, a brilliant neurophysiologist, inquisitor, rigorous, and

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passionate about developing neurophysiological techniques for use in the intraoperative environment and obsessed with the neurophysiology of the motor system. Together with Professor Vahe Amassian, MD, Deletis taught Soto and others a new world by monitoring the motor system, using transcranial electrical motor evoked potentials. In Latin America in those early years, at the beginning of the 1990s, Soto and other pioneering Latin American neurophysiologists, including Brazilians, implemented intraoperative monitoring with somatosensory potentials and continuous and stimulated electromyography in their first cases of tethered cord and scoliosis. In some cases, they added auditory evoked potentials, as in cerebellopontine angle tumors. The need for monitoring the motor pathway has become evident since cases of motor neurological deficits began to be described in which somatosensory potentials remained unaltered. With the lessons learned at NYU, Soto performed for the first time in Chile, in 1999, the transcranial motor electrical stimulation, with the train stimulation technique, with equipment imported directly from Great Britain (Digitimer®). Soto focused on implementing these techniques on his patients in Santiago. Without knowing each other, in different countries, other pioneering neurophysiologists in Latin America were following the same path, such as the Brazilians Ricardo Ferreira, Silvia Verst, and Adauri Camargo, from São Paulo, Martín Segura, from Buenos Aires, and many others who will still be mentioned in this chapter. Those were times when neurosurgeons and orthopedic surgeons did not know about monitoring or had only heard about it in international symposia. Therefore, it was necessary to make them aware of its benefits for patients’ safety and present it again and again in the congresses of these specialties.

Influence of International Societies and Mentors Some international mentors and societies played a crucial role in the development of IOM in Latin America. The mentors who have always been in Latin America giving lectures at courses and conferences are professors Marc Nuwer (University of California), MD, PhD, Jaime López (Stanford University), MD, PhD, and Aatif Husain (Duke University), MD, PhD. All of them have contributed a lot to the dissemination of knowledge in IOM in Latin America, including receiving many Latin American neurophysiologists for IOM training in their institutions. The International Federation of Clinical Neurophysiology (IFCN) and its Latin American Chapter (LAC) have supported every one of the renowned Latin American Intraoperative Neurophysiology Symposia. IFCN’s support has been consistent, not only in allocating funds but and especially in academic support. History must always acknowledge these symposia that

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have motivated many physicians in Latin America to dedicate themselves to this specialty. The other scientific society that has been pivotal is the International Society of Intraoperative Neurophysiology (ISIN). It was founded in 2006 by Vedran Deletis and Beatrice Cioni in Rome, and since then has contributed immensely with valuable guidelines in this discipline. However, it was only in 2009 that an ISIN speaker, Francesco Sala, MD, PhD, a brilliant neurosurgeon from Verona, visited Latin America for the first time, at an event in Porto Alegre, Brazil. Sala motivated many people with one of the first and most robust articles on the evidence that monitoring improves and impacts surgical outcomes: In a historical case-control study, with 50 cases without the use of monitoring and 50 cases with its use, operated by the same team, in strictly matched and comparable patients. Sala has received several neurophysiologists from Latin America at his center and has visited the continent many times after 2009: Chile, Argentina, Brazil (again), and Mexico. ISIN, with its brightest members, began to generously nurture Latin American neurophysiologists with the participation of its members on different occasions and countries. A special section will be devoted later to how ISIN organized one of its Biannual congresses for the first time in Latin America, ISIN Rio 2015.

Special Interest Group (SIG) and IOM Events in Latin America The Special Interest Group (SIG) on IOM of the Latin American Chapter (LAC) of the IFCN (SIG-IOM-LAC-IFCN) was founded in 2009 by Ricardo Ferreira, Martin Segura, Francisco Soto, Francisco Luccas, and Daniel Cibils. Throughout its existence, the SIG has been fruitful and has organized the biannual Latin American symposia: in Montevideo organized by Daniel Cibils (Fig.  1.1), Porto Alegre organized by Ricardo Ferreira and Carlo Domenico Marrone, Viña del Mar organized by Francisco Soto, Buenos Aires organized by Martín Segura, Guadalajara organized by Armando Tello, and Bogotá organized by Jorge Gutierrez. The role of the members of the IOM SIG has been fundamental in organizing and promoting high-level scientific events in Latin America. The SIG and its five founding members have been modified (Fig. 1.2) after the resignation of Francisco Jose Luccas and then Daniel Cibils, incorporating the Chairman of the Guadalajara Symposium, the prominent Armando Tello, representative of Latin America at the IFCN, and then the Chairman of the Symposium from Bogotá, Jorge Gutierrez, past President of the IFCN LAC and current member of the IFCN Board of Directors. In 2015, Ferreira created the Latin American Institute of Intraoperative Neurophysiology – ILANI. It is restricted to his ex-fellows and invited friends from Latin America, USA, and Europe. It aims to promote lectures to the 68 members.

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Fig. 1.1  First Latin American Symposium on Intraoperative Neurophysiology (Montevideo, 2007). (Courtesy of Soto’s personal file)

Fig. 1.2  Special Interest Group on Intraoperative Neurophysiology of the Latin American Chapter of the IFCN. (Courtesy of Soto’s personal file)

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ISIN Rio 2015 After establishing solid academic relationships with the ISIN and becoming active members of this Society, two Latin Americans, Ricardo Ferreira and Francisco Soto, were encouraged to assume a more significant challenge, organize the Biannual Congress and annual Educational Course in Rio de Janeiro. They had to compete against other venues in the world that presented attractive and powerful proposals. However, the ISIN Board elected them in Cape Town, South Africa. In this Congress in the year 2013, Ferreira proudly presented the next venue of the 5th Congress of the History of the ISIN without knowing that it would become one of the best and most vibrant events in History in the field of Intraoperative Neurophysiology. It was a titanic effort, which had to be financed from scratch, in one of the most beautiful and expensive cities globally. Latin America’s reaction was of joy and jubilation to have this opportunity to attend an event of this level in the continent, which was reflected in 400 attendees. Finally, it was a beautiful event lasting one whole week, in a beautiful hotel on Copacabana beach, where joy was breathed and an academic and scientific level that is still remembered worldwide. One of the ISIN Congress lights was born in a breakfast in Istanbul 2014, in one of the Educational Courses of the ISIN. Ferreira, Soto, and the remembered Scientific Committee Chairman of the ISIN at that time, Karl Kothbauer (†), raised the idea of holding a Session on the warning criteria for motor evoked potentials. This idea became a reality at ISIN Rio 2015, by five brilliant speakers: Martín Segura, brilliant neurologist and neurophysiologist from Hospital Garrahan in Buenos Aires, David Mac Donald, Editor in Chief of the IOM Section of Clinical Neurophysiology, Karl Kothbauer, Austrian-born professor at Lucerne in Switzerland, a world-renowned neurosurgeon and direct disciple of Fred Epstein, Louis Journee, leading Dutch neurologist from the beautiful city of the University of Groningen, one of the world authorities on motor evoked potentials and that with Langeloo published the alarm criterion of a decrease of 80% in motor potentials during scoliosis surgery, and Blair Calancie, the author of the threshold criterion in motor potentials. It was a vibrant session, full of scientific discussion that reflected an article in the Journal of Clinical Neurophysiology on this topic; with all the participants at this ISIN Rio round table, this article remains as the Gold Standard. The list of invited professors to ISIN Rio was incredible. It included 34 professors (Fig. 1.3). It was a great effort, but without a doubt, it was rewarded for the mark it left on Latin America.

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Fig. 1.3  Faculty ISIN Rio 2015. (Courtesy of Soto’s personal file)

History of IOM in Brazil An Overview of Late 1980s and Early 1990s In the late 1980s and early 1990s, the study and use of evoked potentials (EP) emerged. Brazilian neurophysiologists interested in the area traveled annually to the United States to participate in courses of the American Society of Clinical Evoked Potentials (ASCEP). In these events, the lectures by Donald York, Aage Moller, and Neil Spielholz on the application of EP in the intraoperative environment aroused the interest of Brazilians. This period coincides with the emergence of magnetic resonance imaging (MRI), a milestone in the advancement of the diagnosis of demyelinating neurological diseases, such as multiple sclerosis (MS). MS represented one of the main outpatient indications for the use of EP. MRI eventually replaced the EP as the first exam for MS diagnosis. Hence, IOM came to renew the use and re-signify the importance of the EP in a new context: the OR. However, it is worth mentioning that the earliest experiences of IOM in Brazil date back to the 1970s. Electrocorticography (ECoG) and direct cortical stimulation (DCS) in epilepsy surgeries have been carried out by professor Raul Marino Junior (Fig. 1.4), MD, PhD, since 1971, at the Institute of Psychiatry (IPQ) of the University of São Paulo (USP) [26]. He learned the methodology with professors Theodore Rasmussen and Wilder Penfield, during his Fellowship in Functional Neurosurgery at Montreal Neurological Institute (MNI), Canada [27].

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Fig. 1.4  Professor Raul Marino Junior, the first Brazilian neurosurgeon to perform awake craniotomies with motor and language mapping. (Source: Marino Jr., Raul. Um cirurgião sob o olhar de Deus: uma introdução às ciências do cérebro, da mente e do espírito. Barueri: Manole, 2020, with permission)

Marino was the first Brazilian neurosurgeon to perform awake craniotomies (Fig. 1.5) with motor and language mapping, initially on his own and later with the collaboration of physiatrist and neurophysiologist Gary Gronich (Fig. 1.6). Meanwhile, the neurologist and neurophysiologist Francisco José Carchedi Luccas (Fig. 1.7) started in 1986 to perform EP in OR for skull base surgeries at Hospital Israelita Albert Einstein (HIAE), in Sao Paulo. He showed some of his cases at the symposia by the Company Berger (1990–1995). From the mid-1990s came a more favorable moment for the expansion of IOM in Brazil: the country’s economic stability, better access to technology, and a greater number of specialists in Neurophysiology besides Epilepsy and EEG. In addition, the use of Neurophysiology in an intraoperative environment in Europe and in the USA was also advancing.

Experience and Reports of Brazilian Pioneers Most of the pioneering neurophysiologists in IOM in Brazil were self-taught, but all of them had a very solid base in Clinical Neurophysiology.

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Fig. 1.5  Preparation for epilepsy surgery with patient awake in 1971, by the team of Professor Raul Marino Junior. (Source: Marino Jr., Raul. Um cirurgião sob o olhar de Deus: uma introdução às ciências do cérebro, da mente e do espírito. Barueri: Manole, 2020, with permission) Fig. 1.6  Gary Gronich, the first Brazilian neurophysiologist to perform intraoperative neurophysiological monitoring in the 1970s. (Source: Marino Jr., Raul. Um cirurgião sob o olhar de Deus: uma introdução às ciências do cérebro, da mente e do espírito. Barueri: Manole, 2020, with permission)

Gary Gronich, MD Physiatrist and neurophysiologist Gary Gronich’s interest in intraoperative neurophysiology dates back to the early 1970s, when he was still a student at USP Medical School (FMUSP). He attended Luccas in intraoperative EEG monitoring in animal models undergoing liver transplantation.

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Fig. 1.7  Francisco José Carchedi Luccas, neurophysiologist who started in 1986 to perform evoked potentials in the operating room. (Courtesy of Luccas’ personal file)

Fig. 1.8 Transoperative electrocorticographic record, performed by Gary Gronich in the 1970s. (Source: Marino Jr., Raul. Um cirurgião sob o olhar de Deus: uma introdução às ciências do cérebro, da mente e do espírito. Barueri: Manole, 2020, with permission)

From 1972, Gronich began to participate in the activities of the Department of Neurophysiology of USP, performing ECoG records in laboratory animals. Short after that, a damage compromised the DCS device that Professor Marino used in his pioneering surgeries. Aware of Gronich skills as a self-taught electronics technician, Marino called him to repair the device and invited him to join the studies on epilepsy surgeries at IPQ. Hence, in mid-1974, they founded CENEPSI, Center for Neuropsychosurgery at USP.  Gronich was responsible for ECoG and DCS (Figs.  1.8 and 1.9) and also

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Fig. 1.9  Brain mapping with electrocorticography and electrical stimulation for epilepsy surgery, performed at HCFMUSP. (Source: Marino Jr., Raul. Um cirurgião sob o olhar de Deus: uma introdução às ciências do cérebro, da mente e do espírito. Barueri: Manole, 2020, with permission)

became head of the newly formed CENEPSI Bioengineering Laboratory. A hundred other specialists joined the team and formed the embryo of what would become USP’s Functional Neurosurgery Division (DNF). In the late 1970s, Gronich became director of the entire IPQ EEG Department and was responsible for restructuring the Service, transforming it into a Clinical Neurophysiology Laboratory. “In addition to ECoG, we also performed DCS on awake patient in surgeries for epilepsy of the temporal lobe and in surgeries for resection of tumors in eloquent areas, talking to the patient during stimulation. We performed DCS with current intensity from 0.5 to 5 mA, pulse duration of 1 ms and frequency from 5 Hz to 60 Hz. We developed several electrodes and probes by hand, always aiming to better adapt to the intraoperative circumstances that we would face. All the electrodes and devices created for the group were developed by me in the bioengineering laboratory of CENEPSI. In 2009, I retired after more than 40  years dedicated to Neurophysiology at IPQ. I made great friendships and also enmities. And I was able to solve part of the immense curiosity that had always motivated me to better understand how the nervous system works”, reported Gronich. Francisco José Carchedi Luccas, MD Francisco José Carchedi Luccas was responsible for introducing EP in OR during tumors resection at cerebellopontine angle, in 1986, at the Hospital Israelita Albert Einstein (HIAE), in São Paulo. Luccas has been performing EEG since 1972 and EP since 1982 in outpatients. In 1986, he started to monitor carotid endarterectomies with EEG and several other types of brain surgeries with SEP, visual evoked potential (VEP) and brainstem auditory evoked potential (BAEP). “The initial difficulties were due to the lack of portability of the equipment at the time and mainly because the surgeons did not know exactly how the

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neurophysiologist could help. They did not accept very well the team with biomedical technicians in neurophysiology. Additionally, it was tiring for the neurophysiologist to stay many hours in the OR while there were other hospital calls to see patients in Intensive Care Units (ICUs) and elective exams. I dedicated myself to IOM from 1986 until 1998 and as I grew older, I got tired of the arduous routine of the OR“, stated Luccas. After Luccas, during the 1990s, Ricardo José Rodriguez Ferreira, Adauri Bueno de Camargo, and Silvia Mazzali-Verst began their practice in an almost simultaneous chronology. Since 2000, many others have emerged: Maria Lúcia Furtado de Mendonça (Rio de Janeiro), Carlo Domênico Marrone (Rio Grande do Sul), Alfredo Torres Castellon (São Paulo), Maria Rufina Barros (Espírito Santo), Rachel de Alvarenga Boy Lanna (Minas Gerais), Karina Maria Alécio de Oliveira, and José Alberto Nunes Sobrinho (Distrito Federal). Ricardo José Rodriguez Ferreira, MD The history of IOM in Brazil is an integral part of the personal and professional history of the physiatrist and neurophysiologist Ricardo José Rodriguez Ferreira. In 1990, Ferreira assumed the service of Electroneuromyography (EMG) and EP of the Association for Assistance to Disabled Children (AACD), in São Paulo. In 1994, he received a mission from the chief spine surgeon Ivan Ferraretto: to study and carry out the first IOM during a spine surgery in a year to come at Abreu Sodré Hospital. Self-taught, initially reading papers and EP books, Ferreira began his research on and soon realized that his main obstacles would be the limitations of equipment and the anesthetic regime. In February 1995, he performed his first IOM: one case of Acoustic Neurinoma resection surgery with the neurosurgeon Jean -Luc Fobe, at Hospital Santa Paula, in São Paulo (Fig. 1.10). It is worth remembering that Fobé has always been one of the greatest enthusiasts and supporters of the use of IOM and that his name is also often mentioned by three other important Brazilian pioneers in IOM, Adauri Bueno de Camargo, Silvia Mazzali-Verst, and Luiz Henrique Cuzziol who, together with Ferreira, constituted the so-called AACD group. Ferreira relied on Jorge Florêncio Cardoso, from the company Alfamedic, to optimize several necessary adaptations in his EMG/EP equipment for the spinal surgery to come. At that time, as MEP did not yet exist, it was mandatory to perform the Wake-up test (Stagnara test). It consisted of an intraoperative clinical motor test created in 1973, which was the gold standard for scoliosis approach. He asked AACD anesthesiologists to study on how to accomplish a total intravenous anesthetic regimen. It was a challenge at the time, since there were no continuous infusion pumps and no shorter half-life drugs to facilitate this activity. Additional difficulties were lack of evaluation of the anesthetic depth (bispectral index – BIS) and absence of neuromuscular block reversals. Thus, in 1995 the AACD team was ready to perform SEP and EMG during the first Brazilian IOM of a spine surgery (Fig.  1.11). Since then, they have

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Fig. 1.10  First IOM performed by Ricardo Ferreira (February 1995): Acoustic Neurinoma resection surgery. (Courtesy of Ferreira’s personal file)

Fig. 1.11  Left: First Brazilian IOM in spine surgery and equipment of the time (at AACD, September 1995). Right: Ricardo Ferreira and the anesthesia and surgery teams. (Courtesy of Ferreira’s personal file)

increasingly improved the protocols and equipment, spreading the knowledge about IOM to the surgeons, stimulating and teaching neurophysiologists about this area of expertise.

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In 1997, Ferreira went to Chicago (USA) to participate in a Congress of an American society exclusively devoted to IOM  – American Society of Neurophysiology Monitoring  – ASNM.  That year, cork-screw needle electrodes were launched, which would revolutionize both the transcranial electrical stimulation and recordings from the scalp. Next, Ferreira encouraged Silvia Mazzali-Verst and Adauri Bueno de Camargo to accompany him to the ASNM Congresses in Philadelphia (1998) and in Denver (1999) (Fig.  1.12). These meetings led the AACD team to familiarize with IOM particularities, in a “step by step” way. Ferreira led many courses and congresses in Brazil and Latin America in the following years (see topics “Special Interest Group (SIG) and IOM Events in Latin America”, “ISIN Rio 2015”, and “IOM Events by SBNC”). These meetings were in the origin of the spread of the IOM in this side of the world. Jaime Lopez, Head of Intraoperative Neurophysiology at Stanford University, was a frequent guest by Ferreira’s meetings. They first met in 2002, during an Fig. 1.12  Ricardo Ferreira and Silvia Verst at the opening ceremony of the ASNM Congress in Denver (1999). (Courtesy of Ferreira’s personal file)

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Fig. 1.13  Jaime Lopez, Ricardo Ferreira, and Charlie Cho at Stanford University, in 2002. (Courtesy of Ferreira’s personal file)

observational training at Stanford University, in Palo Alto-California (USA). On the occasion, Ferreira helped Lopez’s team to carry out their first MEP with transcranial electrical stimulation in an upper thoracic spine surgery (Fig.  1.13). Since then, Lopez has been several times in Brazil to exchange knowledge. In 2018, Ferreira and Segura presented their “Joint proposal of a Conduct Algorithm in MEP alarm in spine deformities” at the IFCN World Congress in Washington (USA). In 2020, in New Orleans (USA), Ferreira’s team has been awarded the prize of “Young Investigator”. Ferreira is a remarkable figure in the history of Brazilian IOM, since almost all pioneers mentioned his influence in their reports. Adauri Bueno de Camargo, MD Adauri Bueno de Camargo is one of the most prominent physiatrists in Neurophysiology in Brazil. From 1994 to 1999, he worked as a Neurophysiologist at AACD, in São Paulo, with Ricardo Ferreira, Luiz Henrique Cuzziol, and Silvia Mazzali Verst. This was the so-called “AACD group”. They formed a group of independent neurophysiologists who worked side by side in some hospitals and separated most of the time. They exchanged many experiences and collaborated whenever necessary. They reported that, in 1996, the neurosurgeon Jean-Luc Fobe, returning from his Fellowship with the renowned surgeon Marc Sindou, in Lyon,

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France, started working at AACD and operating children, especially those with spasticity, submitted to rhizotomy. “One day Fobe came knocking on our door, in the Neurophysiology Department, asking us to assist him at the surgical center. From there, we started to study, investigate and inform ourselves about Intraoperative Neurophysiology. We started to “venture” into the AACD surgical center, relying on Fobe’s goodwill and patience”, reported Camargo. At that time, there was no dedicated or suitable equipment for IOM.  EP and EMG devices were used, configuring the protocols for what was believed to be appropriate. Ferreira soon located a congress in the USA, the 1997 Congress of the ASNM, returning very excited and full of plans. His excitement motivated the “AACD group” to start with their trajectories in IOM. From 1999 to 2001, Camargo specialized in Intraoperative Neurophysiology, at the Institute of Neurology and Neurosurgery, with Vedran Deletis (Department of Neurophysiology), Fred Epstein (Department of Neurosurgery), and Alex Berenstein (Department of Neuroradiology), at Beth Israel Medical Center (Albert Einstein College of Medicine, Yeshiva University, New York). The service offered two fellowship seats annually and Camargo took the seat left by Francesco Sala. At the time, his fellow colleague was Andrea Szelenyi. After 2 years of fellowship, he was invited to remain in the same service, this time training new fellows (Klaus Novak and Sedat Ukatan), supervising and guiding intraoperative monitoring and participating in research activities. In 2003, Camargo received a proposal to set up the Intraoperative Neurophysiology Hospital Service at HIAE in São Paulo and ended up returning to Brazil. He worked at HIAE establishing the first intra-hospital intraoperative neurophysiological monitoring service (although other colleagues had already been practicing IOM in the country, it was performed independently, privately, and there was not yet an “inhouse” hospital service established and entirely dedicated to IOM). Camargo became responsible for the entire Department of Neurophysiology, when Luccas left his position. In 2005, Camargo went to New York accepting an invitation to work with the same group of Neurosurgery with which he had worked at the time of his Fellowship. They had divided the Neurosurgery group after the death of Fred Epstein. Deletis went to the campus at St. Luke’s-Roosevelt Hospital, and Camargo was invited to Montefiore Medical Center, another campus of Albert Einstein College of Medicine. Meanwhile (2005–2011), Camargo kept ties with Brazil through guidance and consultancy to Brazilian professionals in the area, with special attention to Silvia Verst, who had assumed his position at HIAE after his return to the USA. Camargo conducted part of the training of countless IOM technicians in the USA from 2005 to the present. In 2010, he went to work at the New  York University School of Medicine and, in 2012, returned to São Paulo again, where he lived until 2018. In 2019 he returned to New York to work in the IOM Department at New York University, under the leadership of Aleksander Beric. He is actually co-responsible for the Continuing Education in IOM at the institution.

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Silvia Mazzali-Verst, MD, PhD Silvia Mazzali-Verst is, without a doubt, one of the Brazilian intraoperative neurophysiologists with greater national and international prominence. She has published six papers in international medical journals as author and many others as co-author. In 1995, Verst started to work at the AACD with Ferreira. There, she received training in EP with Adauri Bueno de Camargo and Luiz Henrique Cuzziol and became interested in IOM. In 1998, Verst, Ferreira, and Camargo participated in the Congress of the ASNM, in Philadelphia, USA. Since then, Verst started a tireless way to acquire knowledge in IOM. Twice, she has visited the IOM service at the Albert Einstein School of Medicine (New York, USA), coordinated by Professor Vedran Deletis, during Camargo’s fellowship. In 2002, when her first child was born, she sold her Digitimer device to Alfredo Torres Castellon and left IOM and São Paulo for 2 years. She came back in 2004, to take over the department of EMG, EP, and IOM at HIAE. Over the following years, she spent some time learning with Georg Neuloh, at the University Hospital of Bonn (Bonn, Germany), with Andrea Szelenyi, at the University Hospital of Düsseldorf (Düsseldorf, Germany) and with Hughes Duffau, at the University of Montpellier (Montpellier, France). She was also spent precious time with the Brazilian colleague Camargo, at Montefiore Medical Center, in New York, USA (Fig. 1.14). She had participated in the ASNM Congresses and in all the meetings of the ISIN around the world. In 2011, Verst concluded her Physical Degree by the Neurology Department of FMUSP with the orientation of Professor Paulo Henrique Pires de Aguiar. She proposed the use of C5-Cz and C6-Cz as an option assembly for eliciting corticobulbar-­ MEP during skull base surgeries. She is involved with several educational activities: (1) coordination of an IOM Fellowship at Brain Spine Neurofisiologia, (2) invited professor by the Latu Sensu Post-Graduate Program in Neuro-Oncology at the Teaching and Research Institute (IEP) of the Hospital Sírio-Libanês (HSL), and (3) invited professor by Post-­ Graduate Program in Neuro-Anesthesia of FMUSP. At HSL-IEP in 2019, she coordinated the first dedicated course on Awake Craniotomy with a 360° view on this approach, involving anatomy, imaging, anesthesia, surgery, language evaluation, and rehabilitation. The difficulties of the first years of practice were overcome with a lot of creativity and persistence: “In the beginning, we were unaware of the influence of anesthetics, there was still no MEP and the surgeries files were saved on floppy disks. In 2001, I acquired a Digitimer D185 device, but it was difficult to adapt it to my Sapphire four-channels EMG equipment. Besides, there was a shortage of books on the subject. During my visits to the Department of Professor Deletis in New York, I used to stay until late evening, making copies of the papers on the subject. I always came back home with my suitcase crammed with this printed material, many bare needles, cork-screw electrodes and pedicle stimulating probes. After that, I started

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Fig. 1.14  Silvia Verst and Adauri Camargo, at Montefiore Medical Center, in New  York, USA. (Courtesy of Verst’s personal file)

to bring strips and epidural electrodes. Camargo taught me a lot about setting up, protocols and reasoning in IOM”, comments Verst. At the beginning of her career, Verst dedicated herself to Tethered Cord and Scoliosis surgeries at AACD.  In general, most Brazilian neurophysiologists with basic training in IOM tend to be more skillful and focused on spine procedures. Verst is an exception, since she steps herself as passionate for Neurosurgery. “My soul mate in IOM is Maria Rufina Barros, who shares this passion. We were immediately aware of this neurophysiological compatibility when we first met in Croatia during ISIN meeting in 2009”. Her main research interests are in the field of Neurosurgery. Verst’s trajectory in awake craniotomy began in 2007, with the return of the Brazilian neurosurgeon Marcos Vinicius Calfat Maldaun, MD, PhD from his Fellowship at the MD Anderson Cancer Center, in Texas (USA). They developed together the monopolar high-­ frequency technique for awake craniotomies.

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“It is very difficult to be a pioneer. We insisted on our language mapping protocol because we obtained good results for the patients. This led us to develop a better intraoperative language test and to perform different tasks, such as drawing, semantics, due task, writing, visual field, syntax, memory and repetition. We perform tasks tailored to the individual and the region of the brain being operated on. Nowadays, we are pleased to use a dynamic approach and receive visitors in the OR to see our work”, stated Verst in an interview for the Clinical Neurophysiology Practice Journal, 2020. Based on the first 20 pictures that Maldaun had brought from Texas, they validated a language test composed of 420 images among native Brazilian Portuguese speakers [28]. Their language task is called Verst-Maldaun Language Assessment for object naming and semantic, which is available under vemotests.com (more details in Chap. 18). This dedication resulted in four papers about awake craniotomy and language assessment [28–31]. She is also involved in a cryoablation research project being held by Ricardo de Freitas, MD, PhD at the Neurology Department of FMUSP, using an animal model [32]. Their experience was presented at the European Congress of Radiology in 2020. She is proud to be have been part of the team of Evandro de Oliveira, MD, PhD† (until his retirement in 2019). Many other neurosurgeons that directly influenced her career are authors and co-authors in this book. Alfredo Torres Castellon, MD, PhD Alfredo Torres Castellon is a physiatrist and neurophysiologist. He has been working with EMG since 1991. His interest in IOM started in 1999 after his fellowship with Ferreira. “My activity in the IOM area had the fundamental incentive of Ricardo Ferreira. During the 10 years of this partnership, we worked not only in São Paulo, but also explored several regions of Brazil, which did not yet have intraoperative neurophysiologists.”, said Castellon. During 22 years of uninterrupted practice, Castellon contributed to the evolution of IOM in Brazil; held a master’s degree in “Intraoperative Neurophysiological Monitoring in spinal fractures” from the Hospital Santa Casa de Misericórdia de São Paulo; and trained other neurophysiologists in the field. Maria Lúcia Furtado de Mendonça, MD Maria Lúcia Furtado de Mendonça has always been the greatest Brazilian reference in IOM of cardiovascular procedures. Here is her personal account of the beginnings of her practice: “I was fortunate enough to meet Francisco Luccas in 1992, when a multidisciplinary team from HIAE came to Rio de Janeiro (RJ) to assess the coma prognosis of the mother of the former president of Brazil, Fernando Collor de Melo, in the midst of a political impeachment. This event resulted in the beginning of a friendship, companionship and admiration for life.

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In 1993, under the guidance of Luccas and inspiration from Kenneth Jordan, MD (California, USA), I started EEG monitoring in critical patients at Pró-Cardíaco Hospital, in RJ. In that same year, we also started the monitoring of carotid endarterectomies and cardiac surgeries, initially unimodal monitoring, with continuous EEG.  In 1999, we started multimodal IOM (EEG, transcranial doppler, and SEP) for cardiac, aortic, and carotid surgeries. Between 1993 and 2012, approximately 3.500 cardiovascular procedures were monitored at the Pró-Cardíaco Hospital. In 2002, I met Ricardo Ferreira at the Congress of Brazilian Society of Clinical Neurophysiology (SBNC), in Arraial da Ajuda (Bahia) (Fig. 1.15). Ferreira encouraged me to expand the monitoring to neurological and spine surgeries, providing all

Fig. 1.15  Maria Lucia F. Mendonça (left) and Karina Maria A.  Oliveira (right) at the South American Congress of CLA/IFCN, in 2002. (Courtesy of Ferreira’s personal file)

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the support, from the orientation to purchase the equipment to the assistance in surgeries in which I was not self-confident. In 2009, I acquired equipment for monitoring neurological surgeries, which represented a new step in my career”, reported Mendonça. Carlo Domênico Marrone, MD Although root monitoring with EMG in spinal surgeries had been carried out since 1970 in Porto Alegre (Rio Grande do Sul-RS) and EcoG for epilepsy surgeries since 1990, it was only in 1998 that IOM emerged in RS with Carlo Domênico Marrone. At the time, Marrone performed mapping and monitoring of peripheral nerves at São Lucas Hospital of the Pontifical Catholic University of Rio Grande do Sul (PUCRS) with surgeon Jefferson Braga Silva. He used to make his own electrodes with Kirschner wires. In 1999, Marrone began a beautiful friendship with Ricardo Ferreira and started making regular trips to São Paulo to watch his surgeries. In 2000, he participated in the first IOM course at São Lucas Hospital (Porto Alegre), taught by Adauri Bueno de Camargo. In 2001, he held IOM Fellowship at Freie Universität, Universitätsklinikum Benjamin Franklin, in Berlin, Germany. And shortly after his return to Brazil, in August 2001, the first multimodal IOM was performed in RS. It was carried out by Marrone with the neurosurgeon Arlindo D’Ávila, in a lumbosacral spine stenosis surgery. In 2005, at SBNC Congress, in Gramado (RS), together with Ferreira, Marrone held the first Brazilian Symposium on IOM (Fig. 1.16). In 2007, the First Latin American IOM Symposium (Fig.  1.1) took place in Montevideo (Uruguay), chaired by Daniel Cibils, MD. In 2009, the Second Latin

Fig. 1.16  I Brazilian IOM Symposium in the SBNC Brazilian Congress, in Gramado-RS, in 2005. (Courtesy of Ferreira’s personal file)

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American IOM Symposium was held in Brazil, with Ferreira as Chairman and Marrone as Co-Chairman. From that point, the spread of IOM throughout Latin America was gradually increasing. In the teaching field, Marrone has already participated and still actively participates in IOM training of neurophysiologists, having trained so far 11 professionals. Marrone is the current president (2019–2021) of the SBNC. During his tenure, the Continuing Education Project in Neurophysiology was implemented. It consists of weekly online academic meetings, comprising all procedures in neurophysiology. Once a month, the subject is IOM. Karina Maria Alécio de Oliveira, MD Karina Maria Alécio de Oliveira had as a mentor in her training in Clinical Neurophysiology Roberto Low, MD. Like Luccas, Low and Oliveira are Brazilian references in EP. Oliveira concluded IOM Fellowship in 1999 at the Toronto Western Hospital, Canada. Upon her returning to Brazil, she started her practice with difficulties and a lot of self-teaching. Below is her testimony: “My experience and learning are mainly due to the setting up of the IOM Department for brain tumors resection involving eloquent areas at the Hospital de Base do Distrito Federal (HBDF, Brasília-DF). There, I monitored the cases of neurosurgeon Luiz Cláudio Modesto Pereira, MD, PhD. His Awake Craniotomies between 1998 and 2008 were part of this project: “Efficacy of craniotomy with fully awake patient for resection of primary supratentorial tumors in eloquent area” (Fig. 1.17).

Fig. 1.17  IOMs performed by Karina Oliveira in 1998 in craniotomies with fully awake patient for resection of primary supratentorial tumors in eloquent area at the Hospital de Base do Distrito Federal. (Courtesy of Oliveira’s personal file)

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In 2009, I met José Alberto Nunes Sobrinho, MD, who became my partner and great companion in IOM. We founded Stela Clinic and, in 2012, we created an IOM Fellowship in partnership with HBDF and the Foundation for Teaching and Research in Health Sciences of the Federal District (FEPECS). It was a 1 year long, full-time, remunerated fellowship. It was indeed the first Brazilian Fellowship in IOM officially linked to the Ministry of Education (MEC). We trained Andreya Fonseca Cardoso Cavalcanti, MD. And a story that saddens me a lot is that I have never been able to leverage IOM in Functional Neurosurgery as there are companies with commercial interests that take non-medical technicians and software engineers to perform this activity. However, I never stopped studying and I feel ready for the opportunity whenever it comes.” José Alberto Nunes Sobrinho, MD Until 2009, before forming a team with Oliveira, José Alberto Nunes Sobrinho was little known for his experience in IOM. He had been practicing high standard IOM by Sarah Network of Hospitals. “I first learned about IOM at Sarah Hospital in the year 2000, when we performed tibial nerves SEP during scoliosis approaches. We used a Nihon Kohden device and complemented the assessment with a wake-up test. At that time, I read about the Digitimer D185 equipment and soon after, in 2002, Sarah Hospital Brasília acquired one. Yet, we still had a limited number of recording channels. We solved some technical difficulties thanks to Ricardo Ferreira who told us how to obtain boxes with selector keys and extension cables. From that, I was able to perform all other possible neurophysiological modalities. Over time, I looked for better devices that could be used exclusively for IOM. In 2004, in my opinion, the German company Inomed’s equipment was the most modern. At that time, the first Latin American IOM symposium took place. There I met other renowned neurophysiologists who had been dedicating themselves to IOM for years. They also were dealing with national limitations, but with utmost creativity: Karina Alécio, Maria Lúcia Mendonça, Carlo Marrone, Rachel Boy, Alfredo Castellon, Daniel Cibils and Francisco Soto. This group was the embryo for the next Latin American symposia and congresses, when there was an exponential increase in the number of people in the area.”, stated Sobrinho. Maria Rufina Barros, MD It was 1998 when Maria Rufina Barros asked her chief of the EMG Residency at the Clinic Hospital of the Ribeirão Preto Medical School (FMUSP-RP), Wilson Marques Júnior, MD, PhD to contact Ricardo Ferreira. She was willing to do an IOM internship at AACD, in São Paulo. However, at that time, only SEP was performed with a Wake-up Test for scoliosis surgeries.

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After Barros ended her first internship in IOM at AACD, she set with Ferreira that she would return to learn MEP as soon as it would come up. She began her IOM department in Vitória-ES in 1999. Back then, she used a four-channel electromyographer to monitor facial nerve discharges in surgeries for cerebellopontine angle tumor resection. It took her 10 years to return to learn MEP with Ferreira, at AACD. After that, she immediately bought her first IOM equipment with a transcranial motor stimulator. In 2010, due to a request made by Ferreira, Barros was received by Jaime Lopez at the Clinic Hospital of Stanford University (USA). Her third internship in IOM enabled her to improve her practice and protocols, especially in posterior fossa and vascular surgeries. Barros is perhaps the Brazilian Neurophysiologist with greater expertise in IOM for traumatic injuries of the brachial plexus and peripheral nerves in general. She has a peculiar experience in the area as she performs a preoperative EMG planning as part of the IOM in cases of spine, spinal cord, and peripheral nerves IOM. “For about 10 years, our team, composed by surgeons and neurophysiologist, has been doing IOM planning together based on patient preoperative exams. According to the surgeons’ report, the improvement of the result with the use of IOM is unquestionable. Neurolysis and Anastomosis are techniques that have been used for 25 years; the difference highlighted by the surgeons is that now neurophysiology tells them what to do and where to do it”, explains Barros. Just like the rocky road endured by several other pioneers in IOM, Barros’ search for knowledge could not be left out: “Yes, we had to travel a lot, not only searching for symposia, congresses and courses, but also looking for our IOM stuff. We had no option but to buy more delicate manufacture stimulating probes and even the common electrodes outside the country. It was already part of our travel itinerary; we usually placed the order in advance and had it delivered to the hotel. Even after over two decades of IOM in Brazil, we still suffer a lot with the extremely limited supply and variety of material. Nowadays we are no longer allowed to buy the latest products abroad and return back with them, even if we declare them to custom. This bureaucracy to register new material and equipment is something that needs to change urgently. It enormously delays progress and the acquisition of new technologies.” In 2009, Barros attended her first ISIN meeting, in Dubrovinik (Croacia). At this event, she had the opportunity to approach and talk in private with Aage Moller, questioning critically the details of the IOM protocols of the posterior fossa surgeries and showing him her records. After a pleasant and productive conversation on the topic, Moller ended up encouraging the reasoning of Barros and said to her: “we are neurosurgeons, we started this. But you are neurophysiologists and you will do much more and better than us”. Another event that deserves to be mentioned on this trip is highlighted by Barros: “It was when I met Silvia Verst, who challenged me with a series of questions in a

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conversation about IOM during the flight. I believe that I did well because since then we have cultivated a friendship, affection and admiration that I cherish immensely.” Barros owes to Ricardo Ferreira all her training, guidance, and motivation in the area of IOM. She has been participating in almost all the Symposia and Conferences organized by him since the end of the 1990s. It gave her the opportunity to meet with several international personalities of IOM. Finally, Barros could never dissociate her trajectory in IOM from the figure of the renowned neurosurgeon Paulo Melo Jacques, MD, PhD. He has always allowed her to take innovative ideas, techniques, and concepts to the surgical protocols, under the justification of his professional motto: “What matters is the final result, even if it costs us more dedication”. Technicians in Neurophysiology As for the role of non-medical health professionals in the IOM area in Brazil, we emphasize that SBNC recognizes the activity of technicians in Neurophysiology (biomedical, nurses, among others), provided they are directly supervised by a neurophysiologist [33, 34]. The technician is not allowed to indicate, plan, analyze, or interpret the data acquired during IOM. The technician may be trained to assist the neurophysiologist but never to replace him [33, 34]. In Brazil, the training of technicians in Neurophysiology has always been more focused on outpatient procedures (EEG, Polysomnography, and EP). There is a shortage of well-trained and qualified IOM technicians to work in the area. Andrea Broisler Sucena Caivano represents one of the pioneering neurophysiological technical professionals in the IOM field. She is biomedical and has been working as a Clinical Neurophysiology General Technician since 1988 and as IOM technician since 2004. “I did my specialization in Clinical Neurophysiology in 1988 with Francisco Luccas, working for many years with EEG and EP at HIAE, in São Paulo. I first learned about IOM in 2002, when I participated in the IV International Symposium on Intraoperative Neurophysiological Monitoring at Beth Israel Medical Center, in New York. During this period, at HIAE, we used to perform EEG in endarterectomies and BAEP and SEP in brain tumors. In 2004, I did a specialization at St. Luke’s Hospital (New York) with Vedran Deletis and at John Hopkins Hospital (Baltimore) with Adauri Camargo. In 2007, I started working exclusively with IOM with the team of Silvia Verst. As a technical assistant I acquired skills to understand all the neurophysiological tests that are performed during the procedure, assisting the physician responsible for IOM with the setting up and acquisition of the records. “, stated Caivano.

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Academic Training in IOM in Brazil Denise Spinola Pinheiro, MD The neurologist and neurophysiologist Denise Spinola Pinheiro has been coordinating the IOM Fellowship program at the Federal University of São Paulo (Unifesp-SP) for many years now. It is the only current IOM Fellowship offered by a Brazilian public university. “I was a little self-taught. As I was extremely interested in the area, I joined a co-worker, Carmelinda Campos, MD and together we started to study IOM.  We published a paper on neurological endovascular procedures. Afterwards, the university bought an IOM equipment, sponsored by funds from the São Paulo State Research Support Foundation (Fapesp). That enabled us to implement the IOM service. In 2015, I started the Fellowship program, which today has become an official specialization course at Unifesp. Since 2015, we have trained 24 neurophysiologists in IOM.”, reported Pinheiro. Pinheiro, Oliveira, and Jessie Navarro, MD stand as the few Brazilian neurophysiologists with experience in IOM for Functional Neurosurgery, especially in Deep Brain Stimulation (DBS) procedures. Training Challenges Regarding academic training in IOM, there are practically no formal institutional training centers. Over the years, Ferreira, Verst, Marrone, and Pinheiro were responsible for IOM training of many neurophysiologists and technical assistants. Many of their fellows were pioneers in IOM in their states, allowing the spread of the technique throughout Brazil. Paulo Kimaid, MD, PhD (who will be mentioned in a topic ahead) structured an informative course, with intensive and short duration theoretical and practical steps. Recently, training criteria created by SBNC are detailed in Chap. 2. Yet, many neurophysiologists interested in IOM still need to spend some time training outside Brazil. Many IOM departments throughout the USA and in shorter terms in Europe, welcome and tutor colleagues in short (a month) and long term (1–2 years). There is still no consensus on the ideal period of training. Carla Juliana Araújo Ferreira, MD (Belo Horizonte-Minas Gerais) is a young neurophysiologist who can give a testimony on this matter. Her training was based on a mixed educational model, partly done in Brazil and partly abroad. Her training in IOM in Brazil was mentored by Silvia Verst, Andreya Cardoso, and Wilson Scapini, MD. Afterward, Araújo Ferreira went to the United States, where she did a Research Fellow in IOM at the University of Pittsburgh Medical Center with a scholarship from the International Federation of Clinical Neurophysiology (IFCN). Here is her clarifying testimony drawing a comparative parallel between Brazilian education and training abroad.

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“Little by little, I learned that IOM’s pioneers in Brazil took the responsibility of developing programs in order to teach new professionals to work in the area. I started training in IOM in 2016 with the team of Silvia Verst, Andreya Cardoso and Wilson Scapini, who all work in different hospitals in and around São Paulo, hospitals with different quality and complexity. I participated in almost 100 procedures between 2016 and 2017 and at the end of 2017, I went to Pittsburgh for a Fellow with an IFCN scholarship for young neurophysiologists. Along the six-month period, I experienced an immersion in a different reality, but not necessarily more enriching. The level of professionalism of the American medical system is contrasting. Each hospital has its own team, which takes the relationship between surgeons and neurophysiologists to a different level of interaction and quality of communication. The teams are structured with professionals of different levels of training: technicians, non-medical neurophysiologists and neurophysiologists neurologists. Each has a very well-defined role and surgeries of different complexities demand more or less participation of each member. Telemedicine is very well structured. Teamwork is highly organized to allow regular rest for professionals, thus avoiding overload. Practice and research go hand in hand. All in all, the systemic organization is admirable. However, I still think that despite everything, the service provided by the good Brazilian neurophysiologist to the patient manages to be somehow superior. Perhaps because there is no or less intermediation by a technician, perhaps because we are almost exclusively focused on assistance. The person who manages the equipment (press the buttons) is the same person who has full medical knowledge and thus manages to have a broader view, greater interpretative capacity and greater “neuroplasticity” in the protocols. I realized that multimodality was limited under the justification that too much information would end up being difficult to manage, what they call “cognitive noise”, which does not apply to the good Brazilian neurophysiologist. At the end of the day, I see that my training in IOM in different services was complementary and not at all redundant, with different aspects being addressed in each stage of the training. And despite the frequently unfavorable system, or because of it, the good doctor is especially good”.

Evolution of IOM Equipment and Its Arrival in Brazil The evolution of the IOM equipment followed the development of our pioneers. They always brought to Brazil each of the latest models of equipment. “When I started IOM, I used a device that allowed me to perform SEP and, with some adaptations, also a few EMG channels. In 1998, I acquired a 4-channel Dantec device (Fig.  1.18). Afterwards, I ordered a 12-channel device from an Argentinian company to carry out EMG”, stated Ferreira.

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Fig. 1.18  4-Channel Dantec device – Digitimer D185 – switch boxes from Alfamedic. (Courtesy of Ferreira’s personal file)

“In order to enhance recording channels, my husband, a German engineer called Heinrich Verst, built us a shielded cable with 64 twisted and shielded numbered wires. I remember that it was very difficult to find a dealer of touch-proof connectors. The 4 meters-cable allowed us to connect the muscle recording needles at one end and the other end to equipment. It became possible to switch between muscle channels, as required by scoliosis surgery. We enhanced our recordings capability. The cable was very heavy though. Later on, we introduced a switch stimulation box (Fig. 1.19), first created by Vedran Deletis, that had given to me” stated Silvia Verst. Regarding the use of the MEP in Brazil, Ferreira and Silvia Verst brought the first transcranial electric stimulators (Digitimer D-185) in 2001 (Fig.  1.18). “Step by step, we demonstrated to surgeons that there was no longer need to perform the Wake-Up test in scoliosis”, stated Ferreira. “In 2004, a 16-channel IOM device had been brought to HIAE, however, the hospital gave up buying it. I acquired the first 16-channel device in Brazil. And in 2008, Marrone and I acquired the first two 32-channel devices in the country. Today, young intraoperative neurophysiologists cannot even imagine how difficult our daily lives at the OR were at that time. Since then, the equipment has improved a lot. They developed into a dedicated IOM software and greater number of recording and stimulating channels. Currently, there are several companies in Brazil that have electrodes and equipment ready for delivery, with online support and repair services, a real luxury.

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a

b

Fig. 1.19  Stimulation and recording boxes developed by Vedran Deletis and given as a gift to Silvia Verst in 1999, during her first visit. (a) MEP stimulation box connected to Cz, Cz+6 cm, C1, C2, C3, and C4. At that time, six stimulating corkscrew electrodes were placed for every surgery. It was unclear which combination would work better. It was possible to set the pin direction to anode or cathode and then invert them to “normal or opposite”. Only one combination could be used per turn. (b) Recording box with 15 channels and ground electrode. This box was connected to the four-channel EMG machine and it was possible to enable 4 channels for analysis as needed. Thus, all recording cables were “in reach”, and it was easily possible to switch between channels. (Courtesy of Verst’s personal file)

I emphasize that despite this truly simple arsenal and full of adaptations, we carried out procedures within the established protocols and with enormous ethical and technical commitment. We still have these records today”, reported Ferreira.

Brazilian Society of Clinical Neurophysiology (SBNC) IOM Events by SBNC The first IOM courses, symposia, and congresses in Brazil were of paramount importance for the spread of this field among Brazilian neurophysiologists. They were led by Ferreira with the contribution of many others, like Luccas, Mendonça, Barros, Oliveira, and Marrone. • 2000: IOM lecture in the VIII Brazilian Conference on Clinical Neurophysiology (Belo Horizonte-MG), including an IOM Workshop at Hospital Arapiara (Fig. 1.20). • 2002: Session about IOM in the South American Congress of the Latin American Chapter of the International Federation of Clinical Neurophysiology (LAC/ IFCN), in Porto Seguro-BA (Fig. 1.15).

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Fig. 1.20  IOM Workshop at Hospital Arapiara (MG)/VIII Brazilian Conference on Clinical Neurophysiology (2000). (Courtesy of Ferreira’s personal file)

• 2005: I Brazilian IOM Symposium in the SBNC Brazilian Congress, in Gramado-­RS (Fig.  1.16). During this meeting, Luccas, Marrone, and Ferreira achieved to create IOM as an area of interest inside SBNC. • 2007: II Brazilian IOM Symposium in the SBNC Brazilian Congress, in São Paulo-SP (Fig. 1.21). • 2009: XXII SBNC Brazilian Congress (Florianópolis-SC): SBNC IOM Department was created by Andréa Julião de Oliveira, MD, current SBNC president. • Since then, every SBNC Congress has IOM sessions in its scientific program. • 2011: XXIII SBNC Brazilian Congress/VI LAC/IFCN’s Congress, in Punta Del Este (Uruguai): the first SBNC examining board for IOM certification exam was composed. • 2013–2015-2017: Relevant IOM sessions in the SBNC congresses in Rio de Janeiro (2013), Natal (2015), and Goiânia (2017). • In 2019, in São Paulo, was held the XXVII SBNC Brazilian Congress/VII LAC/ IFCN’s Congress. Several international renowned specialists were there. All

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Fig. 1.21  II Brazilian IOM Symposium in the SBNC Brazilian Congress, in São Paulo, in 2007. From left to right: Soto, Oliveira, Sobrinho, Ferreira, Marrone, Cibils and Castellon. (Courtesy of Sobrinho’s personal file)

IOM lectures were full. It took place exactly 14 years after the first Symposium, which had gathered few Brazilians interested in IOM. Nowadays, there are over a hundred neurophysiologists performing IOM in Brazil. Development of IOM Department at SBNC Paulo André Teixeira Kimaid, MD, PhD first became interested in IOM in 2004. He declares himself as self-taught. In 2011, Kimaid assumed the presidency of SBNC. During his tenure, the first SBNC examining board for IOM certification exam was composed. It approved the first candidates ever: Ricardo Ferreira and Rafael de Castro, who had recently arrived from his Fellowship with Aaatif Hussein at Duke University, North Carolina (USA). The first examining board was comprised by Maria Lúcia Furtado de Mendonça (RJ), Karina Maria Alécio de Oliveira (DF), Carlo Domenico Marrone (RS), and Rinaldo Claudino (SC). Kimaid participated in the examining boards of SBNC from 2012 to 2019. He could count on Castro for heading the IOM scientific department of SBNC during

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this period. As an interesting note, Castro and José Alberto Campos da Silva Júnior, MD were the first neurophysiologists to perform IOM in Northeastern Brazil. In 2015, Kimaid assisted the Neurology Technical Chamber of the Federal Council of Medicine (CFM) to write and publish a resolution that regulates IOM practice in Brazil [33, 35]. At this same year, he started teaching IOM. His course has the peculiarity of compressing the classes in short-days period with observational surgeries. Since 2018, Kimaid has been part of the IFCN Educational Committee. As part of his interest in teaching, Kimaid managed to publish the first Brazilian book in IOM in 2019.

Current Status of IOM in Brazil and Latin America Every neurophysiologist who joined this world had a mentor who encouraged them to follow this path. This path is still under construction as it is the last frontier of clinical neurophysiology. There are areas of darkness that are not yet understood, complete areas of the nervous system that cannot yet be monitored; a person has to have a unique spirit to persevere in a discipline like this, with a grueling operating room and no schedule. All Latin American countries have already joined this discipline. There are several working groups; without a doubt, tens of thousands of cases of the most varied pathologies are carried out per year. But it is important to emphasize that there are threats to the healthy development of the IOM. Intraoperative neurophysiology is a medical act that benefits a patient facing a complex surgery: Reason why the physician should carry out the monitoring. A person with in-depth knowledge of neurophysiology, neuroanatomy, and systemic factors can speak correctly with an anesthesiologist and surgeon. When the situation justifies the temporary or permanent suspension of surgery, it is an enormous responsibility; the neurophysiologist cannot abandon the patient. Intraoperative neurophysiologists should try give their best to teach new generations in this discipline, developing gentle, rigorous, patient-centered professionals. Conclusion IOM’s arrival in developing countries faced many more difficulties than its introduction in Europe and in the United States. In Brazil, its practice has become more expressive in the last fifteen years, after the registration of equipment and materials to carry it out. The availability of the new technology has been accompanied by disorderly growth, resulting in concern about the indications, the training of those who carry it out and also how it should be carried out. Knowledge in intraoperative neurophysiology in Brazil continues to flourish, thanks not only to the dedicated and persistent pioneers, but also to the young neurophysiologists who have emerged in the area.

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Multimodality is a term that refers not only to the diversity and complementarity of neurophysiological techniques used in IOM, but also characterizes the versatility and creativity of its practitioners. We hope that this chapter will inspire surgeons, neurophysiologists, anesthesiologists, and technologists to work together and in a “multimodal way”, using a lot of creativity, versatility, and scientific knowledge to reduce postoperative neurological deficits.

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21. Hicks RG, Burke DJ, Stephen JP.  Monitoring spinal cord function during scoliosis surgery with Cotrel- Dubousset instrumentation. Med J Aust. 1991;154:82–6. 22. Burke D, Hicks R, Stephen J, Woodforth I, Crawford M.  Assessment of corticospinal and somatosensory conduction simultaneously during scoliosis surgery. Electroencephalogr Clin Neurophysiol. 1992;85:388–96. 23. Taniguchi M, Cedzich C, Schramm J. Modification of cortical stimulation for motor evoked potentials under general anesthesia: technical description. Neurosurgery. 1993;32(2):219–26. https://doi.org/10.1227/00006123-­199302000-­00011. PMID: 8437660. 24. Kothbauer KF, Deletis V, Epstein FJ. Motor-evoked potential monitoring for intramedullary spinal cord tumor surgery: correlation of clinical and neurophysiological data in a series of 100 consecutive procedures. Neurosurg Focus. 1998;4(5):e1. 25. Calancie B, Harris W, Brindle GF, Green BA, Landy HJ. Threshold-level repetitive transcranial electrical stimulation for intraoperative monitoring of central motor conduction. J Neurosurg. 2001;95(Suppl. 2):161–8. 26. Amaro JWF. A história do Instituto de Psiquiatria do Hospital das Clínicas e do Departamento de Psiquiatria da Faculdade de Medicina da Universidade de São Paulo. Arch Clin Psychiatry (São Paulo). 2003;30(2):44–71. 27. Marino JR.  Um cirurgião sob o olhar de Deus: uma introdução às ciências do cérebro, da mente e do espírito. 1st ed. Barueri-São Paulo: Manole; 2020. 28. Verst SM, de Castro I, Scappini-Junior W, de Melo MN, de Oliveira JR, de Almeida SS, Alvarez NRC, Sucena ACB, Barros MR, Marrone CD, Maldaun MVC.  Methodology for creating and validating object naming and semantic tests used by Verst-Maldaun Language Assessment during awake craniotomies. Clin Neurol Neurosurg. 2021;202:106485. https:// doi.org/10.1016/j.clineuro.2021.106485. PMID: 33476885. 29. Verst SM, de Aguiar PHP, Joaquim MAS, Vieira VG, Sucena ABC, Maldaun MVC. Monopolar 250-500 Hz language mapping: results of 41 patients. Clin Neurophysiol Pract. 2018;10(4):1–8. https://doi.org/10.1016/j.cnp.2018.11.002. PMID: 30619979; PMCID: PMC6312792. 30. Mathias RN, de Aguiar PH, da Luz Oliveira EP, Verst SM, Vieira V, Docema MF, Calfat Maldaun MV. “Next Door” intraoperative magnetic resonance imaging for awake craniotomy: preliminary experience and technical note. Surg Neurol Int. 2016;7(Suppl 40):S1021–7. https://doi.org/10.4103/2152-­7806.195587. PMID: 28144477; PMCID: PMC5234280. 31. Verst SM, Melo MND, Caivano AS, Fonseca US, Mathias LR, Alves TV. Awake surgery versus VEP in tumors of visual pathway: case report. Interdiscip Neurosurg. 2020;20:100675. 32. de Freitas RMC, Caldas JGMP, Verst SM, Hoff AO, Bezerra Neto JE, Fragoso MCBV. Crossed-­ probes cryoablation for the treatment of a sclerotic vertebral metastasis abutting the spinal canal. J Vasc Interv Radiol. 2020;31(2):284–5. https://doi.org/10.1016/j.jvir.2019.11.006. PMID: 31997752. 33. Diário Oficial da União de 01 de março de 2016,seção 1, p.71. Resolução CFM 2136-2015 de 11 de dezembro de 2015. 34. Kimaid PAT. Monitorização Neurofisiológica Intraoperatória: Conceitos Básicos e Técnicas. 1st ed. Brazil: Thieme Revinter; 2019. p. 4. 35. Recommendation document for the exercise of Clinical Neurophysiology in Brazil. Executive Committee  – Brazilian Society of Clinical Neurophysiology  – Affiliated to the Brazilian Medical Association. https://sbnc.org.br/legislacao/

Chapter 2

Intraoperative Neurophysiological Monitoring in Brazil: Regulatory Aspects, Training, and Evidence Level Carlo Domênico Marrone and Andréa Broisler Sucena Caivano

Abbreviations AMB Brazilian Medical Association CDC Código de Defesa do Consumidor CFBM Conselho Federal de Biomedicina CFBM Federal Council of Biomedicine CFM Conselho Federal de Medicina CME Comissão Mista de Especialidades – Joint Specialties’ Commission CRM Conselho Regional de Medicina EBM Evidence-Based Medicine EBP Evidence-Based Practice EEG Electroencephalography EMG Electromyography GRADE Grading of Recommendations Assessment, Development and Evaluation IONM Intraoperative neurophysiological monitoring IT Information technology MEP Motor potentials NP Clinical Neurophysiology C. D. Marrone (*) Brazilian Clinical Neurophysiology Society, Porto Alegre, RS, Brazil Intraoperative Neurophysiological Monitoring, Department Coordinator of Hospital da Criança Santo Antônio, Porto Alegre, RS, Brazil Universidade Federal de Ciências da Saúde de Porto Alegre - UFCSPA, Porto Alegre, RS, Brazil Clínica Marrone, Clinical Neurophysiology, Porto Alegre, RS, Brazil e-mail: [email protected] A. B. S. Caivano Biomedical Technologist, Brain Spine Neurofisiologia, São Paulo, São Paulo, SP, Brazil © The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 S. M. Verst et al. (eds.), Intraoperative Monitoring, https://doi.org/10.1007/978-3-030-95730-8_2

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NPh Neurophysiologist OR Operating room RCT Randomized controlled trials SBNC Brazilian Society of Clinical Neurophysiology SSEP Somatosensory evoked potentials TA Technical assistant

Introduction Clinical neurophysiology (NP) analyzes the generated or provoked signals present in tests such as electromyography (EMG), electroencephalography (EEG), polysomnography, EEG video, visual, auditory, somatosensory evoked potentials (SSEP) of upper and lower limbs, and motor potentials (MEP). It aims to assist in the diagnosis of several pathologies by assessing the central and peripheral nervous systems. IONM combines in real time several tests according to the profile of each surgery and is individualized to patient needs. Tests are performed in a continuous and interspersed manner for an accurate and updated evaluation, meaning in multimodality. Frequently there is a short time opportunity for multifactorial data review before the reaction of the surgeon. It means that it is of cornerstone importance that the neurophysiologist (NPh) provides the best accurate analysis possible. IONM fundamental goals are to avoid and reduce the risk of postoperative neurological deficits, to help the surgeon identify ambiguous neurological structures (e.g., tumor or normal brain? tumor or normal spinal cord?) and reversible neurophysiological changes. Hence, surgery has become safer since damage can be defined early on and the surgeons´ reaction can prevent deficits. It has a pedagogical role for the team involved in the surgery, especially for surgeons, who can master their skills, by identifying functional/physiological abnormalities related to their acts. This process will ultimately benefit the patient. There are essential requirements for a safe IONM.  First, IONM is a medical procedure performed by a NPh. Initial steps include clinical evaluation, analysis of preoperative tests, planning with the surgeon and the anesthesiologist the best strategy for the approach. NPh is responsible for the correct neurophysiological protocol planning and set-up, placement of needles and special electrodes (which demands knowledge of anatomy and physiology), connecting and checking wires, cables, and system, and ensuring that electrical safety and grounding steps were properly carried out. Planning steps include the correct allocation of the system in the crowded OR, where many people are circulating, and other electrical equipments are functioning. The NPh should properly communicate with the other members of the surgical and anesthesia team. Interpretation of IONM alterations should start an immediate interventional cascade. It is fully dependent on the ability of the NPh to promptly exclude technical errors, anesthesia influence, clinical lability (like decreased mean blood pressure or SO2, hypercapnia), limb ischemia, and positional nerve compression, among others.

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Medical Legal and Ethics Aspects IONM is well established in Brazil according to the Federal Board of Medicine (Conselho Federal de Medicina  – CFM) by resolution No. 2136, from 11th of December, 2015 [1]. We point out some of its important issues: • Art. 1. “Intraoperative neurophysiological monitoring is a medical act”. • Art. 2. “The doctor is not authorized to perform surgical procedures with intraoperative neurophysiological monitoring conducted by a non-physician”. • Art. 6. “The surgeon is not authorized to perform intraoperative neurophysiological monitoring concomitantly with the surgical procedure”. The above-mentioned resolution also states that “Acts that support the performance of IONM may be shared with other professionals. These professionals might promote equipment setup, placement and removal of electrodes under on-site supervision by the physician in charge”. The role of technicians in the scope of INOM is discussed in item 4. Yet, there is a civil law that states that any physician can perform any medical procedure [2]. Ethically it is clear that only skilled professionals should perform complex procedures like IONM, which directly affects patient’s health. The most used example of this contradiction is if a non-specialized physician submitted a patient to a cardiac surgery. This physician is legally allowed to do that, according to law 3.268/1957, but it would be ethically reprehensible. Hence, the physician would be submitted to a lawsuit for malpractice, because of any impairment caused to the patient. Last but not least, qualification control should start with hospitals, clinics, health insurance operators, and healthy managers [2]. Therefore, although this is a technical and highly specialized book, one cannot fail to contextualize the responsibilities of all those involved in patient care. In Brazil, from the legal standpoint, civil liability in the medical field is generally governed by the Consumer Protection Code (Código de Defesa do Consumidor – CDC) [3]. Special attention should be paid to Article 14 and paragraph 4: “Art. 14. The service provider is liable, regardless of guilt, for the compensation of the damage caused to customers for defects in the provision of the services, as well as for insufficient or inadequate information about their fruition and risks. [...]. [...] § 4  – Personal accountability of self-employed professionals shall be determined through the verification of guilt”. According to CDC, in cases of medical error, physicians shall be responsible for the damage caused if proved guilty because of malpractice, recklessness, or negligence. Hospitals, for example, are accountable for the damage caused regardless of proof of guilt, objectively in joint liability [3]. Just as there is joint civil liability of health insurance operators due to malpractice, i.e., “The health insurance operator and the benefits’ administrator are jointly liable for the damage caused to beneficiaries, since both are part of the service supply chain in the consumption relationship” [4].

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Additionally, hospitals and operating room (OR) managers (nurses/physicians) and healthcare personnel fail to inhibit medical material dealers to provide technicians to operate a system, as if it were IONM. This situation violates articles 1, 2, and 6 of the CFM resolution 2136/15 above-mentioned [1]. Besides, it is an illegal practice of medicine as described in the Brazilian penal code, Article 282. It identifies a criminal action as being the act of practicing a profession without authorization from the competent board or outside the limits imposed by the legislation [5]. The Brazilian Society of Clinical Neurophysiology (SBNC), aiming to assist the health assistance chain, i.e., physicians, hospital clinical and technical directors, and health insurance operators and administrators, issued Alert Statement 001/2020 [11]. It recalls normative resolution 2136/15 on the action of IONM and its legal malpractice consequences [1].

Which Medical Professional Is Qualified to Perform IONM? The law 3.268/1957 states in its article 17 that “physicians may only legally practice medicine in any of its branches or specialties, after prior registration of their titles, diplomas or certificates under the Ministry of Education and Culture and under the Regional Board of Medicine (Conselho Regional de Medicina – CRM), in their due jurisdictions” [2]. It is required for the medical professionals to have proper training while dealing with a highly specialized area. To perform IONM they should master the knowledge of neuroanatomy, neuropathology, neurophysiological tests (instrumentation, electrical safety, application, and interpretation, etc.), anesthesia, and surgical approaches. Therefore, the most skilled and legally certified medical professional to perform IONM in Brazil is the clinical neurophysiologist. Certification by competent boards ensures that proper qualification has been achieved. The Brazilian Medical Association (AMB) has granted the Brazilian Society of Clinical Neurophysiology (SBNC) the duty to apply a proficiency test in this area of activity for decades [6]. The resolution by the Federal Board of Medicine 2148/2016 decrees CME (Comissão Mista de Especialidades – Joint Specialties’ Commission) from January 2016 in Article 5 states that “The CME will only recognize a medical specialty with a minimum of two-year training time and area of activity with a minimum of one-­ year training time, with a mandatory minimum annual workload of 2880  h”. Moreover, in paragraph 2, it clearly states that “The competence matrix from which the time of medical specialty training or area of activity in AMB training programs accredited by a medical specialty society, shall be approved by the CME...”. These requirements are contemplated by the SBNC, which provides a proof of knowledge based on the matrix of competence as determined by the CFM, granting the necessary expertise to the clinical NPh to perform IONM [7, 8]. Regarding medical colleagues who are not clinical NPh and are performing IONM, in Brazil, their performance is a medical act. There is no contention among

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physicians of different specialties, but we must conceptualize terms, so that we practice what we are empowered to perform, especially, but not only, in Head and Neck Surgery and Otorhinolaryngology. They perform laryngeal recurrent and facial nerves mapping, for which they have received proper training during medical residency. Yet, it should be considered totally different from the complex and multimodal tests performed by a NPh, which are included in the term IONM.

Mapping Versus Monitoring There should be a comprehensive understanding of the terms “Monitoring” and “Mapping”. In Portuguese, the words “monitorizar” or “monitorar” can be used without any distinction. They mean to do surveillance, to monitor, control, supervise, assess, and inspect. “Mapping”, on the other hand, refers to making the map of, representing an area defined in a map, and in biology to locate and determine the relative distribution of the different parts of a whole [9]. From a neurophysiological point of view, these terms have different but complementary meanings [10, 11]. Monitoring refers to the multimodality and simultaneous neurophysiological techniques aiming to evaluate several neurological functions, i.e., somatosensory evoked potential, motor evoked potential, brain stem auditory evoked potential, electroencephalogram, electrocorticography, free running electromyography, triggered electromyography, bulbocavernosus reflex, etc. Among these techniques, several mappings of peripheral and central nervous system structures are included, such as mapping of the spinal cord dorsal column, medullary and brainstem nucleus, fourth ventricle floor, direct cortical and subcortical mapping for motor, language and cognitive eloquent areas, nerve roots, peripheral and cranial nerves, etc. Hence, Mapping is only a single part of a “world” represented by the act of monitoring. In Brazil, a clinical neurophysiologist spends 2880 h of training in “monitoring”. It is remarkable the difference with a training course of a particular mapping technique, like for laryngeal recurrent nerve, which duration reaches at most 270–280 h.

How to Teach IONM? Proper training in IONM is a current concern worldwide. IONM is growing faster than the capability of training enough physicians. As a complex procedure that involves several types of neurophysiological tests, it takes time for the physician to build skills. Regarding how a physician should be trained in IONM some concepts are fundamental: (a) The trainer (institution and/or individual) should have one or more personnel in-charge, with unquestionable experience, proficiency, and with certification from the legal Board (SBNC) [1, 6].

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(b) Provide the appropriate means to conduct the training, with dedicated equipment and proper supplies, surgical approaches in different fields of Medicine (neurosurgery, orthopedics, vascular, head neck and otorhinolaryngology, and peripheral nerves). (c) Respect the workload and the competency matrix determined by the certifier (SBNC) [7, 8]. (d) Theoretical classes on basics and advanced IONM clinical discussions. (e) Provide a face-to-face and ongoing teaching/learning program. That is, the student should be in the OR time enough to fill the necessary number of supervised procedures and to discuss the multifactorial events happening during the approaches. The learning curve in IONM requires the student’s presence in OR, handling the device, performing, and interpreting the neurophysiological tests. These requirements make online training impossible and inadmissible. Hence, IONM visualization through a virtual way, even if the surgery is taking place “in the room next door”, is only demonstration, never training. Finally, training is an almost individual task, requiring a maximum of two students per monitoring. It is necessary for better learning purposes, and mainly for patient’s safety not to have a crowdy OR. The above-mentioned criteria are not feasible during a “weekend” model of training, in which a group of 5–10 people huddle together to watch, not to participate in the neurophysiological procedure. “Weekend” training is not suitable for any neurophysiological modalities, like EMG, EEG, and EP. Most frequently it suits only the coursegiver pocket.

What Is the Role of Medical Assistants/Technicians in IONM? The Federal Board of Biomedicine (Conselho Federal de Biomedicina – CFBM) edited the Resolution 245/2014 on this subject [12]. Hence, the medical and the biomedical federal boards clearly stated in their resolutions that IONM is a medical procedure, and that the technical assistant (TA) can assist on IOM performance under on-site medical supervision. TA may assist in terms of equipment, tests performing and electrodes placing and removal. They are not allowed to carry out the planning, decision making, analysis, and interpretation of tests according to the resolutions of regulatory agencies [1, 12]. The TA must be in the OR throughout the entire procedure [13, 14]. TA needs to have proper IOM skills and training. It is ideal to have a degree in any Health area like Biomedicine, Nursing or Physiotherapy, which provides knowledge and experience in patients care. Besides, knowledge of the anatomy and functions of the nervous system (Table 2.3) and knowledge of the electrophysiological

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parameters (Table  2.4) are required for optimal performance. In addition to the degree, TA’s specific certification in IONM is recommended according to the standards of practice of each country. The sole Brazilian professional representation board that regulates the scope of TAs in IONM is the Federal Council of Biomedicine (CFBM). They edited the Resolution 245/2014 [12], which states: • “Art. 1: It is a duty of the Biomedical Professional to act under medical supervision in Transoperative Neurophysiological Monitoring, operating specific equipment for the activity and using electrophysiological methods such as EEG, EMG and SSEP to monitor the integrity of specific nerve structures during surgery.” • “Art. 2: The practice of the professional activity for Transoperative Neurophysiological Monitoring requires a specialization course, duly registered and approved by the Ministry of Education. The minimum disciplines should include Neuroanatomy, Neurophysiology, Basic and Advanced Neuropathology, Theory of Surgical Techniques, Applied Technologies and practical internship in Transoperative Neurophysiological Monitoring services duly registered and under professional supervision and Sanitary Surveillance.” Thus, the legally qualified biomedical is absorbed by specific segments of the labor market, naturally those related to diagnosis, research, and education, with the operation/handling of biomedical equipment and systems, and their participation in IONM is regulated by resolution 245/14 [13, 14]. In daily practice, TA arrives in the OR in advance to prepare the equipment and listed supplies. They set up the equipment, placing it in the room in the best spot not to interfere with other systems, adjusting boxes and cables. Under supervision of the NPh, he/she separates the electrodes that will be used and sets all the material organized and ready for placement. He/she assists in the placement of electrodes as planned by the NPh, allocating wires and cables in the best way so as not to harm patients and not to run the risk of being removed during patients positioning and along the procedure. He/she ensures all connections are properly set in the boxes according to the selected protocol and measures impedance. After baseline recordings, he/she follows the surgery, adjusting the system boxes, and assists with recordings when necessary. When the surgery is finished, the TA turns off the equipment, disassembles and puts everything away in the case, removes the electrodes, assisting until the end of the surgery. The IONM system might be operated by TA under NPh supervision. For this task, it is required that the TA is trained in the software and hardware and masters knowledge about signals, waveforms, stimulation, filters, artifacts, electrode impedance and positioning, and troubleshooting. As Skinner and Holdefer say, the teamwork enhances results [15].

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Is There Evidence and Level of Recommendation for IONM? The experience of each physician or group of physicians in a given situation undoubtedly has its value in the handling decision-making. However, it is necessary to refine medical reasoning, to reduce the biases which may occur and, at the same time, produce more comprehensive knowledge. Thus, evidence-based medicine (EBM), a term coined by Guyatt in 1991, using epidemiological principles from Cochran and Feinstein, aims to improve medical reasoning. In 1992, the Evidence-­ Based Working Group proposed a systematic process of discovering, assessing, and using research to support clinical decision-making [16]. Jenicek (1997) organized the principles for this systematic process, that is, (a) formulation of a clear clinical question based on the patient’s problem which needs to be responded to, (b) searching the literature for other relevant articles/sources of information, (c) critical assessment of the evidence, (d) selection of the best piece of evidence, (e) linking evidence with clinical experience, knowledge, and practice, (f) implementation of useful findings in clinical practice, (g) assessment of the overall performance and implementation by the MBE professional, and (h) teaching other physicians how to practice EBM [17, 18]. In the hierarchical pyramid of the evidence quality classification (Chart 2.1) and strength of recommendation (Table 2.1), controlled and randomized clinical trials have been at the top for many years, especially in the comparative assessment of

Chart 2.1  Evidence-based practice (EBP) and how we can relate it to GRADE (Grading of Recommendations Assessment, Development and Evaluation)

2  Intraoperative Neurophysiological Monitoring in Brazil: Regulatory Aspects… Table 2.1  Quality of evidence [25]

Class I Class II Class III

Table 2.2  Strength of recommendation [25]

Type A Type B Type C Type D Type E Type U

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One or more prospective, blind and well-designed controlled studies One or more well-designed clinical studies (case-control, cohort, etc.) Expert opinion, non-randomized historical control and case reports

Strongly positive based on Class I or very strong Class II Positive in Class II Positive based on strong Class III consensus Negative based on conflictive or inconclusive Class II Negative based on ineffective evidence No recommendation based on insufficient data or divided expert opinion

randomized and non-randomized (observational) studies. In recent years, a great movement has been taking strength to consider how the study is conducted, identifying the specific sources of bias and the confidence limitations regarding the treatment effects [19, 20]. Although very relevant, randomized controlled trials (RCT) that assess treatment/outcomes may have serious limitations resulting from biases that have not been duly identified. On the other hand, observational studies for treatment and outcomes, which would normally have lower weight in the hierarchy of evidence quality classification, if well adjusted for confounding situations, may play an important role in supporting the evidence [21]. The evidence quality assessment by the GRADE (Grading of Recommendations Assessment, Development and Evaluation) method is used by several agencies (WHO, BMJ, NIH, etc.) and is a key element for better understanding in systematic reviews, randomized controlled trials, and non-randomized controlled (observational) trials [22]. GRADE aims to provide a high, moderate, low, or very low Evidence Certainty rating through domain assessments that serve as a grading tool. The domains are divided into risk of bias, inconsistency, indirect evidence, inaccuracy, and publication bias, among others. RCTs enter the GRADE method with a high level of evidence quality but depending on how they behave in the domains (risk of bias, inconsistency, indirect evidence, inaccuracy, publication bias, etc.), they may be downgraded, whereas the opposite may occur with observational studies [21]. Most studies on IONM are conducted as observational (they are not randomized controlled trials) and class I evidence is not found, being classified as class II and III – Tables 2.1 and 2.2 [19, 23]. However, as Sala (a neurosurgeon by the way) argues, much of the evidence used in neurosurgical treatment cases are also

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classified as class II and III (acute spinal cord injuries, aneurysms, traumatic head and brain injury, benign tumors, etc.). Thus, the level of evidence-based medicine in IONM is no worse than what is found in neurosurgery in general [23]. There is little research with comparative designs on the effects of treatment [21]. An explanation has been attributed to ethical and legal restrictions to perform randomized studies on IONM in surgeries with high risk of neurological injury [24]. Therefore, as an example, it would not be ethical/legal to conduct a research in scoliosis approach to: (a) assess the outcome of absence or presence of spinal cord injury having one group making use of IONM and not the other, (b) making surgeons and neurophysiologists blind to IOM alterations. Therefore, as Holdefer and Skinner stated, comparative studies on the effectiveness of IONM on outcomes are both necessary and urgent. One cannot accept new technologies such as IONM as a “fad”/“hype cycle” (all that is new is good!), nor should we think that it will never be possible to design new studies based on the knowledge gathered by IONM [21, 23]. Concerning RCTs and IONM, there may be ethical/legal restrictions for surgeries with greater potential of causing harm to the nervous system. For those with less potential of harm there might be the possibility of RCT designs, despite the difficulties regarding trial costs and number of patients. If RCT is not possible, observational comparative studies can be conducted with all scientific rigor (e.g., using GRADE) to improve methods and, mainly, to adjust confounding factors (Chart 2.1). As Howick et  al. stated, data records with perspectives of monitored and unmonitored controls offer the possibility of enough statistical power to detect small reductions in the already very low incidence of iatrogenic injuries [25]. A multi-centric collaboration in an attempt to constitute an observational cohort study might represent an excellent alternative to the difficulties of conducting a controlled trial in IONM [25]. As a matter of fact, given the expertise of countless colleagues among us, why not do this in Brazil and Latin America? (Table 2.3). The 2021–2022 SBNC directory’s recommendations for the several types of IONM were under construction by the time of release of this book. The process includes the systematic review phase according to the GRADE method with the elaborated questions under discussion using the PICO method  – Patients, Table 2.3  Description of basic knowledge for TA

Decubitus Median, sagittal, frontal, transversal planes Central and peripheral nervous system – which are the structures Anatomy of the brain – frontal, parietal, temporal, and occipital lobes – spatial vision and main functions Sympathetic and parasympathetic autonomous system – basic function Peripheral nervous system – basic function Anatomy of cranial pairs, muscles to be needled

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Interventions, Comparison and Outcomes [26]. Recommendations and degrees of evidence of the American Society of Clinical Monitoring dated 2013 are available elsewhere [17].

 emote or On-Site Neurophysiologist? From Dream to Reality R in Brazil Nowadays, the possibility of assisting the patient with the most diverse and modern technologies is a fact, even if one does not have them all in one place. Telemedicine is a practice of distance medicine, whose interventions, diagnoses, treatment decisions, and recommendations are based on data, documents, and other information transmitted through telecommunications systems. It can contribute in an important way to patients’ well-being as Tel Aviv Declaration [27]. In Neurology there are areas supported by adequate technological and care-­ related infrastructures, which can be safely applied via teleneurology, such as the Neurovascular area (with its Stroke units) and Neurointensive care. According to Maldonado et al. (2016) telemedicine has an interdisciplinary nature, requiring integration from different fields of knowledge, like information technology (IT), telecommunications, equipment development, security protocols of data transmission, etc. [28]. INOM is inserted in the context of modern technologies which greatly assist patients and the anesthesia-surgical teams and, in many countries, is remotely performed [29]. However, technical conditions (the dream) are not readily available for remote IONM via telemedicine in Brazil and many other countries, at least nowadays (reality) (Table 2.4). The topic has already led to heated discussions. Even though remote INOM is carried in some places around the world, one must respect the particularities of each country. After a careful review and peers´ discussion, SBNC decided to strongly recommend in-site NPh (in the OR) – IONM. This complex topic was analyzed in different perspectives to improve the SBNC level of recommendation, as shown below. Table 2.4  Basic understanding requirements of electrophysiological parameters

What is electrical activity? What is amplitude? What is an electrode? What is potential? What is an amplifier?

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Remote IONM IONM, similarly to anesthesia, is traditionally performed by an in-site physician. Most important, classical proof of the efficacy of IONM in surgeries according to class I and II evidence was established in this traditional model, i.e., NPh in the OR [30].  hich Would Be the Best Way to Convey IONM in a Remote Technique W (Dream)? In the USA, there is a rule guide for remote IOM detailing physician supervision. It describes each participant’s role, including which media might be used for external communication among them [29]. Yet, there is no consensus on the most suitable way to collect, transmit, supervise, etc., data in IONM.  Some even suggest that supervision could be done via mobile phone (call, text message, chat, WhatsApp, etc.), whereas others criticize this situation fervently [29, 31]. For EMG outpatient examination, an attempt has been made to establish a protocol via telemedicine. It required installation of real-time capture cameras with accurate focus on needle placement, sound registration, and data image/charts of the system screen, among other requirements. It proved to be an ineffective tool for a correct diagnosis decision [32]. Comparisons between remote IONM with the “telestroke initiative” were held by Skinner and Sala [31, 33–36]. They pointed out that the main concern in a stroke situation is deciding whether to use a thrombolytic agent, whereas in IONM there is “an ongoing flow of neurophysiological data integrated to the surgical context that is in constant change”. Regarding remote IONM, difficulties like data confidentiality, exposure of medical data in communication systems, and adoption of the in-site-remote-physician real-time connection should be overcome [31]. For ethical reasons, the patient should be offered the same technical conditions (including personnel and others), either at in-site or in-remote physician assessment [37]. Hence, IONM should be interpreted in both endings of the chain by skilled physicians specialized in neurophysiology, allowing real-time full access to images and sounds from the OR, and encompassing at least the following [38]: 1. Operating table with patient positioning. 2. Wiring and cabling of IONM equipment and IONM screen in real time. 3. Verbal communication between the physicians involved in IONM and the anesthesiologist, without disturbing the ongoing surgery. 4. Straightforward view of the anesthetist screen for immediate access to data on mean arterial pressure, oximetry, capnography, heart rate, etc. 5. Straightforward communication, that is, sound and image from surgical team. 6. Visualization of surgical field through cameras placed on light spots and/or on microscopes.

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 hat Is the Ideal Distance from the OR? Should the Physician In-Charge W Be Inside or Outside the Same Hospital Where IONM Is Taking Place? Could He/She Be Out of Town, Outside the State or Abroad? How Many IONMs Could be Supervised Simultaneously by the NPh In-Charge? The acceptable distance which the PHh could keep from the OR (we must never forget that IONM should be patient-centered) and the number of simultaneous IONM one physician could carry out are very controversial. The American Academy of Neurology conducted an e-mail survey asking neurologists about the volume, types of cases, duration, number of simultaneous cases, and location of the monitoring physician [39]. Among those who responded to the survey, 86% did it locally, 37% of which did it only inside the OR, 65% were close-by, entering the room if necessary, and it was observed that some did both (sum greater than 100%). Out of the 23% who did it “online”, 15% did it only remotely. Most neurologists who conducted the remote cases did 2.2 cases at a time. People who monitored locally, performed many more intracranial cases whereas those who did remote monitoring had typically more spinal cases. Dormans, 2010, in reference to remote IONM, did the following questions [40]: (a) “How well can an individual outside the OR interpret fluctuating IONM data and develop a plausible explanation for this? (b) How is it possible for a remote professional to deliver an appropriate level of surveillance if multiple cases are being monitored? (c) How can an individual who has never done IONM and who is at a distance from the OR have or develop the necessary skills and expertise to make accurate and reliable decisions? (d) What happens if remote connectivity is lost? (e) What forensic accountability will be taken by the remote professional in case of misinterpretation, negligence, etc.?” What Is the Reliability of IONM Performed by Telemedicine? If communication interruption via connection means even in the best centers happens, more so would it in developing countries [36]. Thus, there may be a serious breach in the neurophysiological procedure safety, especially if it happens at a crucial moment of the surgery. Even if the above-mentioned situations do not occur (dream), some crucial issues about communication and reliability between the anesthesia-surgery-­ neurophysiology teams should be considered. According to the Joint Commission on Accreditation of Healthcare Organization, communication dysfunction has caused medical errors, though in sentinel events, 65% of the time between 1995 and 2004 [41]. Yet, neither the usage of any sophisticated technology in order to enable a remote IONM, nor any telemedicine support and devices, even if well applied, could replace personal interaction. Easy communication between specialists is what ultimately reduces and avoids errors [36, 42].

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An IONM intervention cascade can be summarized by the following sequence: performance of test, interpretation of findings, communication between the team, intervention, and outcome [42]. For this cascade to really work, an essential element is trust between peers during surgery. It may sound simple, but it is of vital importance and must be established long before a possible moment of crisis (e.g., signal loss in the MEP [36, 42]. The clear dialogue between doctors follows the same line, both “spoken” and visual/gestural, especially in urgent situations, because straightforward communication between physicians through posture, gestures, expressions, visual contact, etc., helps in the interpretation and adds meaning to the information being shared [43]. Therefore, familiarity between teams in the OR is also a factor that has influence on good performance, significantly reducing interruption in the surgical flow and leading to fewer errors per case [44]. There is evidence, according to Neilly [45] that communication between teams in the OR and awareness of what is happening goes along with better patient outcomes. Skinner et al. [42] believe that despite good intentions, professionals outside the OR can be frustrated by hindrances that block essential medical information, inadequate ability to deal with a given situation, burden of multiple supervised cases, and insufficient technology. They may have difficulty in collaborating with teams during surgery and reduced awareness of the severity of the threatening situation. These conditions may affect IONM reliability, even when the NPh is present in the room. So, how can one expect reliability with the NPh at a distance or when IONM is done by an unskilled person? Although technological barriers exist, especially in a country of the size and diversity such as Brazil (low-speed and unstable internet, instability of electricity; electrical interference of the OR in IONM equipment, etc.) it is expected that in the future such difficulties could be overcome. Yet, it is not only a matter of better communication infrastructure, enabling better data transmission (the dream), but also of what can be effectively accomplished to ensure the total safety of the patient (reality). Additionally, there is the lack of skilled personnel to be overcome worldwide (reality).

Conflict of Interest It is important that institutions ensure good medical practice for their patients, supervising to prevent malpractice and surgical approaches from being performed by non-experts and not properly trained personnel. A tough issue is the relation between medicine, business, and profit. Any relationship involving people (physicians and their patients), institutions (hospitals), dealers, and healthcare companies should practice the four principles of bioethics: (a) beneficence, (b) non-maleficence, (c) autonomy, and (d) justice. Withdrawing from this way might result in losing the focus on the patient and on the relief from his/her ailments. Hence, the doctor-patient relationship should always be based on

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trust, honesty, and best possible evidence for handling the illness. It should exclude external interferences which may lead to improper care. There has been a growing interest from system manufacturers and medical suppliers in IONM worldwide. It has resulted in better devices, stimulators, probes, and electrodes. Yet, in Brazil, some companies, aiming to increase their profits, sell supplies and provide “monitoring operators” included in the price. Most frequently those operators are non-medical personnel or physicians without proper skills. In this situation a relevant question arises: If there is a bad outcome, whose responsibility, is it? Usually, the surgeon, hospital, and healthcare insurance are issued to pay for the damage. It is strongly recommended that the service supplier be included in this equation.

Conclusion By now we cannot take the risk to perform remote IONM in Brazil and in many other countries. We shall be careful not to mistake “IONM expansion”, meaning more skilled physicians, with increasing business profits at the expense of patient safety. Finally, this chapter aimed to bring up tough issues that are usually left behind in textbooks, but strongly interferes with daily work. Bringing them to real life context, where the main actors of the play are (patients, surgeons, NPh, hospital managers, professional councils, health care insurance, and regulatory agencies), may contribute to the reflection on how to improve patient care.

References 1. Medicina CF.  RESOLUÇÃO N° 2.136, DE 11 DE DEZEMBRO DE 2015  – Disciplina o procedimento de monitorização neurofisiológica intraoperatória como ato médico exclusivo. Diário Oficial da União. 2016, 01 março;Ed. 40:70. 2. Brasil. Lei 3.268/1957 artigo 17. 3. BRASIL.  Lei n°.8.078 de 11 de Setembro de 1990: Código de Defesa do Consumidor. Disponível em: http://www.planalto.gov.br/ccivil_03/leis/l8078.htm. Acesso em: Mar. de 2017b. 4. Código de Defesa do Consumidor Arts. 7°, parágrafo único; 25, § 1°; e 34, todos do CDC. Entendimento do TJDFT de 15/01/2020. 5. Código Penal – Decreto-Lei n° 2.848, de 7 de dezembro de 1940, artigo 282. 6. www.sbnc.org.br/titulos (edital de concurso para obtenção do certificado de área de atuação em neurofisiologia clínica). 7. Resolução do Conselho Federal de Medicina 2148/2016,portaria CME 01/2016 (www.sbnc. org.br/informativos/22-­02-­19). 8. www.sbnc.org.br/titulos (matriz de competência). 9. https://www.infopedia.pt/dicionarios/lingua-­portuguesa/mapear 10. www.sbnc.org.br (newsletter sbnc n° 20 – 10 de abril de 2020 – Alerta 001/2020). 11. https://www.infopedia.pt/dicionarios/lingua-­portuguesa/monitorar

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12. Resolução do CFBM 2457/2014. http://crbm1.gov.br/novosite/wp-­content/uploads/2013/12/ RESOLU%C3%87%C3%83OCFBM-­n%C2%BA-­245.2014.Monitoramento.pdf 13. https://crbm1.gov.br/site2019/wpontent/uploads/2021/03/Manual_do_Biomedo_2021_V4.pdf 14. Nuwer MR.  Regulatory and medical-legal aspects of intraoperative monitoring. J Clin Neurophysiol. 2002;19(5):387–95. 15. Skinner AS, Holdefer RN.  The intraoperative neurophysiological monitoring team. Neurophysiol Neurosurg. 2020;44:607–21. 16. Evidence-Based Working Group. Evidence-based medicine. A new approach to teaching the practice of medicine. JAMA. 1992;268:2420–5. 17. Jenicek M.  Epidemiology, evidenced-based medicine, and evidence-based public health. J Epidemiol. 1997;7(4):187–97. 18. Cartiel LD, Póvoa ED. Medicina Baseado em Evidência: Novo Paradigma assistencial e pedagógico? Interface-Comunicação, Saúde, Educação. 2002;11:113–32. 19. MacDonald DB, Skinner S, Shils J, Yingling C. Intraoperative motor evoked potential monitoring – a position statement by the American Society of Clinical Monitoring. Clin Neurophysiol. 2013;124:2291–316. 20. Djulbegovic B, Guyatt GH. Progress in evidence-based medicine: a quarter century on. Lancet. 2017;390(10092):415–23. 21. Holdefer RN, Skinner AS.  Evidence-based medicine and intraoperative neurophysiology. Neurophysiol Neurosurg. 2020;43:607–21. 22. Guyatt GH, Oxman AD, Vist GE, Kunz R, Falck-Ytter Y, Alonso-Coello P, Schünemann HJ, GRADE Working Group. GRADE: an emerging consensus on rating quality of evidence and strength of recommendations. BMJ. 2008;336(7650):924–6. 23. Sala F. Intraoperative neurophysiology is here to stay. Childs Nerv Syst. 2010;26(4):413–7. 24. Nuwer MR, Emerson RG, Galloway G, Legatt AD, Lopez J, Minahan R, et  al. Evidence-­ based guideline update: intraoperative spinal monitoring with somatosensory and transcranial electrical motor evoked potentials: report of the Therapeutics and Technology Assessment Subcommittee of the American Academy of Neurology and the American Clinical Neurophysiology Society. Neurology. 2012;78(8):585–9. 25. Howick J, Cohen BA, McCulloch P, Thompson M, Skinner SA.  Foundations for evidence-­ based intraoperative neurophysiological monitoring. Clin Neurophysiol. 2016;127(1):81–90. 26. Guyatt G, Rennie D, Meade M, Cook D, editors. Users’ guides to the medical literature: a manual for evidence-based clinical practice. American Medical Association; 2015. 27. Declaração de Tel Aviv sobre responsabilidades e normas éticas na utilização da telemedicina [Internet] 1999. 28. Maldonado JM, Marques AB, Cruz A. Telemedicine: challenges to dissemination in Brazil. Cad Saude Publica. 2016;32(Suppl 2):e00155615. 29. Gertsch JH, Moreira JJ, Lee GR, Hastings JD, Ritzl E, Eccher MA, et al. Practice guidelines for the supervising professional: intraoperative neurophysiological monitoring. J Clin Monit Comput. 2019;33(2):175–83. 30. Emerson RG, Husain AM.  Blurring of local and remote practice models threatens IOM’s future. Neurology. 2013;80(12):1076–7. 31. Skinner SA, Aydinlar EI, Borges LF, Carter BS, Currier BL, Deletis V, et al. Is the new ASNM intraoperative neuromonitoring supervision “guideline” a trustworthy guideline? A commentary. J Clin Monit Comput. 2019;33(2):185–90. 32. Simmons SC, Moore DP, Wells J. Evaluation of technical approaches to tele-­electromyography via internet protocol networks. Telemed e-Health. 2007;13(1):33–9. 33. Wechsler LR, Tsao JW, Levine SR, Swain-Eng RJ, Adams RJ, Demaerschalk BM, et  al. Teleneurology applications: report of the telemedicine work Group of the American Academy of Neurology. Neurology. 2013;80(7):670–6. 34. Sarfo FS, Adamu S, Awuah D, Ovbiagele B. Tele-neurology in sub-Saharan Africa: a systematic review of the literature. J Neurol Sci. 2017;380:196–9.

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35. Martins SC, Pontes-Neto OM, Alves CV, de Freitas GR, Filho JO, Tosta ED, et al. Past, present, and future of stroke in middle-income countries: the Brazilian experience. Int J Stroke. 2013;8(Suppl A100):106–11. 36. Skinner S, Sala F. Communication and collaboration in spine neuromonitoring: time to expect more, a lot more, from the neurophysiologists. J Neurosurg Spine. 2017;27(1):1–6. 37. Skinner S.  Patient-centered care model in IONM: a review and commentary. J Clin Neurophysiol. 2013;30(2):204–9. 38. Stoecklein VM, Faber F, Koch M, Mattmuller R, Schaper A, Rudolph F, et al. Optional real-­ time display of intraoperative neurophysiological monitoring in the microscopic field of view: avoiding communication failures in the operating room. Acta Neurochir. 2015;157(11):1843–7. 39. Nuwer MR, Cohen BH, Shepard KM. Practice patterns for intraoperative neurophysiologic monitoring. Neurology. 2013;80:1156–60. 40. Dormans JP. Establishing a standard of care for neuromonitoring during spinal deformity surgery. Spine. 2010;35(25):2180–5. 41. Joint Commission on Accreditation of Healthcare Organizations. National patient safety goals for 2005 and 2004, 2006. Available at: https://www.jointcommission.org/assets/1/6/2006_ Annual_Report. Accessed 3 Aug 2016. 42. Skinner S, Holdefer R, McAuliffe J, Sala F. Medical error avoidance in intraoperative neurophysiological monitoring: the communication imperative. J Clin Neurophysiol. 2017;7:1–7. 43. Solet DJ, Norvell JM, Rutan GH, Frankel RM.  Lost in translation: challenges and opportunities in physician-to-physician communication during patient handoffs. Acad Med. 2005;80:1094–9. 44. ElBardissi AW, Wiegmann DA, Henrickson S, Wadhera R, Sundt TM III. Identifying methods to improve heart surgery: an operative approach and strategy for implementation on an organizational level. Eur J Cardiothorac Surg. 2008;34:1027–33. 45. Neily J, Mills PD, Young-Xu Y, et al. Association between implemen- tation of a medical team training program and surgical mortality. JAMA. 2010;304:1693–700.

Chapter 3

Muscle Motor Point Atlas and Needling Pitfalls Bruno Nogueira da Silva and Tae Mo Chung

Abbreviations CMAP compound muscle action potential EMG electromyography IOM intraoperative monitoring M muscle mMEP muscle motor evoked potential MU motor unit TES transcranial electrical stimulation

Motor Point Concept The motor point concept as we will apply in this section will have a practical purpose and will be referred to the intramuscular region with the highest density of motor plates (motor plate zone). This region rich in motor plate terminals is the preferred neurophysiologic target for measuring the electrical phenomena of motor units. Its privileged position near the region of onset of depolarization of the muscle fiber produces less phase cancellation effect and higher recording amplitudes translating finally to a better signal-to-noise ratio. Extramuscular motor point, a term applied to the region of entry of the motor branch in the muscle belly, does not correspond anatomically to the region of the B. N. da Silva (*) Clinical Neurophysiologist by Brain Spine Neurofisiologia, Jundiai, SP, Brazil T. M. Chung Clinical Neurophysiology Coordinator, Physical Medicine and Rehabilitation Department at the Clinical Hospital of University of São Paulo Medical School, São Paulo, SP, Brazil © The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 S. M. Verst et al. (eds.), Intraoperative Monitoring, https://doi.org/10.1007/978-3-030-95730-8_3

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motor plate zone and has other practical purposes (e.g., phenolic chemo denervation and application of functional electrical currents for rehabilitation). Despite the availability of practical manuals on the subject, the conceptual confusion between these different muscle sub-regions and the absence of specific anatomical and histological research of the regions of concentration of plaques per muscle in the body make attempts to formulate these so-called motor point maps inaccurate [1, 8, 9]. Considering these limitations, we have drawn up a small suggested topographical guide for positioning muscle needle recording electrodes targeting the motor plate zone.

Production of Muscle Potentials This subject has already been covered in other chapters. We will go through some basic concepts that will help you understand how the recording of muscle potentials can be optimized. The nomenclature of intraoperative monitoring (IOM) sometimes uses the term compound muscle action potentials (CMAP) for both muscle action potentials generated by transcranial electrical stimulation (TES) discharged in the central nervous system and potentials originating from direct stimulation of peripheral nerves (peripheral CMAP). Yet, a distinction is reasonable and already stablished [13] since the methodology applied for generating the peripheral CMAP and muscle motor evoked potentials (mMEP) are different. Peripheral CMAP are obtained by a single pulse while mMEP generally requires a synchronized “bombardment” of excitatory potentials in the lower motor neuron. As the stimulus intensity increases, a progressive number of motor units (MU) are recruited in an almost linear fashion until the total number of MUs is reached (supramaximal stimulation). By TES, the sequence of stimuli causes recruitment of fractions of the MUs at the motor point and is triggered from the first to the nth pulse (usually 3–7 pulses). The amount of MUs recruited per pulse is variable and theoretically the same unit can be recruited at different moments within the train of stimuli provided the absolute refractory time of the neuron involved in impulse generation has passed. Additionally, spontaneous electromyography (EMG) activity recordings are also dependent on proper needling.

Muscle-Potentials Generators (the Motor UNIT) The depolarization of the MU is the elementary phenomenon that will produce the muscle potentials (CMAP and mMEP). MU is the peripheral motor functional unit composed of the body of the second motor neuron (located at the anterior horn of the spinal cord), its axon, neuromuscular junction (motor plate), and all the muscle fibers it innervates. The amplitude of a CMAP, mMEP and spontaneous EMG activity recording is influenced by the amount of muscle fibers per MU of the muscle in question, the average diameter of the muscle fibers, and the spatial distribution of the MU within the

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muscle belly. Each muscle in the body has a quantitative pattern of muscle fibers per MU and the greater this number, the larger the size of the MU. Thus, one MU can supply 6–10 muscle fibers in the orbicular eye muscle to hundreds of fibers as in the bicipital muscle [7]. The area of motor fibers influenced by a particular motor neuron is called the MU territory and varies depending on the muscle [17], with an estimated diameter of 5–10 mm in the biceps brachii [16]. As for muscle fiber size, we know that appendicular muscles of the upper and lower limbs have an average fiber diameter of 40–50 and 50–60 μm, and a smaller number in facial muscles (20–30 μm diameter/ fiber) [2, 14]. Thus, reduced recording amplitudes are expected in smaller muscles. These concepts can help to understand the extreme variation in morphology between the different stimulus trains according to the muscle studied, reinforcing the importance of bringing the recording electrode as close as possible to the motor point region for the best electrical representation of the muscle in question. In this way, the sum of the MU potentials recorded after a stimulation will determine the amplitude of the final CMAP or mMEP. The deflagration of the action potential of each MU is of the all-or-nothing type. Thus, an isolated MU of great amplitude that is close to the recording electrode and that has its excitability varying between stimuli (or eventually becoming difficult to obtain as the anesthetic fading phenomenon evolves) can become a source of concern during surgery and eventually triggers a false-positive alarm.

Recording Electrodes The proximity of the recording electrode to the generator source according to the generator electric dipole and conduction volume theory influences the amplitudes and morphology of the recorded responses in different ways. The types of electrodes available for muscle recording have been covered in the EMG Chap. 11. Here we will reinforce the electrical generators recording theory according to the electrodes available and how their proximity to the muscle and motor point can influence the amplitudes and morphology of the potentials. Available for motor recordings are surface electrodes, insulated and non-­insulated needle electrodes. In surface recording a larger amount of distant MU fibers contribute to the potential [15]. Each type of needle electrode has different recording characteristics as in Table 3.1. Although not well studied, the area of recording of non-insulated needles occurs throughout the whole needle surface. The region of recording is along the entire Table 3.1  Characteristics of recordings according to electrode type Electrode Monopolar insulated needle Concentric needle Single fiber needle MacroEMG

Recording surface 640 μm 150 and 580 μm 25 μm Un-insulated distal 15 mm of needle

Recording area 0.12–0.34 mm2 (10–20 fibers) 0.07 mm2 (10–20 fibers) 0.0005 mm2 (2 muscle fibers) Large 300–2000 fibers

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–

O

+

E

C D

A B

Fig. 3.1  Potential generators in relation to source generators. (A, B): near-field bipolar recording, (C, D): far-field bipolar recording, (A, E): near-field monopolar recording. (D, E): far-field monopolar recording. (This figure was published in Daniel Dumitru, Machiel J Zwarts, Anthony A. Amato (Editors), Electrodiagnostic medicine, 2nd ed. Chapter 2 Electrical sources and volume conduction, Page 28, Copyright Elsevier (2002). Reprinted with permission)

needle and the resulting potential is an average of the electrical fields in proximity to the entire needle denudated surface. According to the theory of conduction volume and electric dipole recording, assemblies embracing more isopotential lines and closer to the electrical generators record higher values of electric dipole voltage (Fig. 3.1). Thus, the monopolar or near-field reference assembly (A-E and B-E) will exhibit potentials of higher amplitudes, followed by the bipolar near-field assembly (A-B). The lowest amplitudes would be registered in the bipolar far-field (C-D) and monopolar far-field (C-E or D-E) assemblies. These last two assemblies would be representative of the recording method with short (non-insulated) subdermal needles. Beyond the concept of isopotential lines, the closer the point chosen for the study of the motor point (the main generator of the muscle electric dipole, due to containing the highest concentration of motor plates), the greater the chance of recording more robust CMAP/mMEP. The distance between the generating unit (MU motor plate zone) and the capture electrode is a very important component for higher CMAP/mMEP amplitudes (Fig.  3.2). It relies on Faraday’s electric field law

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a

6 mm

b

c

d

20 V 5 ms

Fig. 3.2  Muscle Fiber Motor Unit Territory. Position of the recording needle in relation to the muscle motor point directly relates to CMAP/mMEP amplitude and EMG activity recording. Muscle fibers belonging to one MU are randomly distributed within a 6 mm-oval territory. Four separate CMAP waveforms (all representing the same MU) are recorded from four different locations: close to (A) or within the MU (B-D). The more the recording tip is located within the MU territory (B-D), the greater the resulting potential. (This figure was published in Daniel Dumitru, Machiel J Zwarts, Anthony A. Amato (Editors), Electrodiagnostic medicine, 2nd ed. Chapter 2 Electrical sources and volume conduction, Page 72, Copyright Elsevier (2002). Reprinted with permission)

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(F = kQq/d2), which states that the magnitude of the circulating electrical field is directly related to the area enclosed in the loop. Hence, the amplitude of the recorded potential is directly related to the current density, which decreases with an increase in distance from the generator [6]. The greater the distance between the needle and the muscle motor point, the smaller the amplitude of the recorded potential. This principle substantiates the optimized positioning of needles near the electrical generator during any IOM recording. An important and under-discussed aspect is the effect that bare and insulated needles have on recorded muscle activity and CMAP/mMEP.  In general, larger recording surfaces result in slighter smaller potentials. Although larger electrodes will obviously record from a larger area of volume conductor, they will “average out” different contributions from individual MUs [6]. Yet, insulated needles or hook-wire electrodes selectively record over the distal tip area. There is an absence of specific studies on needles differences in IOM. Hence, a parallel can be established with the concepts gained from the electromyography (EMG) laboratory. Monopolar needles and macro-EMG needles have similar recording areas as 13–15  mm-bare needles [10]. Experiments with progressive Teflon denudation (thus enlarging recording surface) of reusable EMG monopolar needles points to impairment of spontaneous muscle activity and recruitment pattern analysis [3].

Obese Patients The muscle electric dipole field in response to stimulation attenuates exponentially as the distance between the record electrode and the generating muscle fibers increases (Faraday’s 2nd law). Signal attenuation will be higher in the presence of thicker adipose tissue, which will enlarge this distance. Jahangiri [11] studied 13 patients comparing the use of paired 13 mm and paired 18 mm, 25 mm, 37 mm, and 50 mm insulated needles for recording mMEPs from the rectus femoris muscle. Records were obtained in 12 patients (92.3% of cases) with 37 and 50 mm insulated needles and in only one patient with 13 mm needle. Recordings through the 37 and 50 mm needles increased the chances of acquiring MEPs even with lower TES thresholds. Kim et al. [12] showed a relationship between obesity and the risk of false positives, possibly related to small mMEPs.

 orphology and Amplitude of Motor Potentials as a Function M of the Position of the Needles in the Muscle Belly The central positioning of the motor plate in muscles is strategic and provides a better dispersion of the action potential bidirectionally along the muscle fiber membrane. Although there are anatomic scattered motor plates throughout the muscle

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body, the zone of greatest concentration is generally located near the midpoint of the muscle belly. The motor plate location within a muscle is directly influenced by the muscle morphology [18]. Histological studies with acetylcholinesterase staining are gold-­ standard for analysis but are scarce. The presumed location of the motor point in a given muscle is in the middle of the muscle belly, especially in fusiform muscles [4]. In longitudinal muscles such as sartorius and gracilis the motor plate zones tend to be more distributed in a scattered manner along the entire long muscle belly. In unipennate muscles, a transverse band rich in motor plates has been found in the middle of the muscle, whereas in bipennate muscles the motor plate band would tend to be concave [2]. A more comprehensive understanding of muscle anatomy and motor plate distribution is not the scope of this chapter.

Relationship Between CMAP and mMEP Peripheral nerve stimulation can be used to measure pharmacological neuromuscular junction blockage. A four-stimulus repeatedly applied results in equal number of CMAPs if there is no blockage. Degree of blockage will be inferred by the number of acquired CMPAs. For example, 2 CMAPs in 4 stimulus represents 50% blockage. Establishing the comparison between CMAP and mMEP improves IOM quality in many aspects, for example, during peripheral nerve approach (Chap. 31). If there is no proper previous EMG study, identifying atrophied muscles by peripheral nerve stimulation in operating room allows to consider better strategies for recording, such as adding muscles to the protocol or changing the insertion point of the needles. Another way to correlate CMAP and mMEP is to perform supramaximal peripheral nerve and TES stimulation. The comparison between them would predict the quantity of MUs elicited. For example, by corticonuclear MEP it is supposed that only one-fifth of the motor pathway is activated by TES [5]. Moreover, if only low amplitude CMAP can be recorded, most probably there will be equally low amplitude mMEP. It is the expected situation for small or atrophied muscles, or for inadequate needles placement. Last but not least, there is an unpredictable pattern of atrophy within a MU and among MUs.

Conclusion As sophisticated and complex as IOM might be, it does not preclude from very basic concepts of neurophysiology. IOM comprises several steps that must be observed individually. The technique of electrode placement is a fundamental one since repositioning is frequently impossible once the procedure has begun. The goal is to elicit the best, the greatest, and more well-defined mMEP, CMAP, and EMG

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activity as possible. It optimizes the recording using basic concepts regarding electrical generators and conduction volume theories. Needle placement should be the closest to the region of greatest concentration of motor plates as possible. Thus, understanding the different muscle morphologies provides ballast for the needling technique. The accumulation of knowledge will point to the most effective types of needles for intraoperative muscle recordings. Costs versus benefits should not be overlooked. At present, there is a lack of uniformity of opinions and practice regarding IOM needle selection. Muscle Motor Points M. frontalis (Picture 3.3) Origin: Skin of the eyebrow. Insertion: Joins the occipital muscle in the aponeurotic galea. Innervation: Facial nerve Action: Pulls the forehead skin upward, wrinkling the forehead. Active electrode: Pupillary line in the middle of forehead Morphology: Wide muscle with parallel fibers.

Depth 0.5 cm

M. Occipitalis (Picture 3.4) Origin: Occipital bone. Insertion: The two venters come together, inserting into the aponeurotic galea. Innervation: Facial nerve (VII cranial pair) Action: Pulls the forehead skin upward, wrinkling the forehead. Active electrode: Three centimeters above the superior nuchal line. Morphology: Wide muscle with parallel fibers. Depth: 0.5 cm

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M. Orbicularis oculi (Picture 3.5) Origin Orbital portion: medial palpebral ligament, frontal, and maxillary bones. Pre-septal portion: medial palpebral ligament and lacrimal ridge. Pre-tarsal portion: medial palpebral ligament (lateral border). Insertion Orbital portion: orbital cutis on maxillary, frontal, and zygomatic bones. Pre-septal portion: middle layer of the lateral palpebral raphe. Pre-tarsal portion: innermost layer of the lateral palpebral fold. Innervation: Facial nerve (VII cranial pair). Action: Closes the eyelids and wrinkles the skin around the eyes. Active electrode: Directs the needle externally to the eyeball. Morphology: Wide muscle with circular fibers. Subcutaneous depth

M. Levator labii superioris alaeque nasi (Picture 3.6) Origin: Frontal process of the maxilla. Insertion: Nose wing and medial portion of the orbicular muscle of the mouth. Innervation: Facial nerve (VII cranial pair). Action: Discrete elevation of the upper lip and the nose wing (dilates the nostril). Active electrode: At the midpoint of the lateral sulcus formed by the nose wing. Morphology: Long muscle with parallel fibers. Depth: 0.3–0.5 cm

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M. orbicularis oris (Picture 3.7) Origin: Most originate from the perioral skin and from the incisive fovea of the jaw and mandible. Insertion: Skin and mucosa of the lips. Innervation: Facial nerve (VII cranial pair). Action: Closes the mouth and protracts the lips. Active electrode: Approximately one centimeter from the labial border. Morphology: Wide muscle with parallel fibers. Depth: 0.5 cm

M. Mentalis (Picture 3.8) Origin: Mentonian fossae above the mentonian tubercle Insertion: Skin of the chin. Innervation: Facial nerve (VII cranial pair). Action: It wrinkles the skin of the chin and folds the lower lip. Active electrode: One centimeter lateral to the midline of the face, between the labial line and the lower border of the mandible. Morphology: Short muscle with parallel fibers. Depth: 0,5–1 cm

M. Platysma (Picture 3.9) Origin: Lower edge of the mandible. Insertion: Skin of the neck, clavicle, and anterior face of the first rib. Innervation: Facial nerve (VII cranial pair). Action: wrinkles the skin of the neck, slightly lowers the jaw, and lowers the angle of the mouth. Active electrode: Multiple possible points arranged between the inferior border of the mandible and the superior border of the clavicle (from its sternal end to the acromial end). Morphology: Wide muscle with parallel fibers. Subcutaneous depth

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M. Genioglossus (Picture 3.10) Origin: Internal surface of the mandible, in the upper genian spine, just above the geniohyoid muscle. Insertion: Tongue body and lingual aponeurosis. Innervation: Hypoglossal nerve (XII cranial pair) Action: Mainly protrudes the tongue, but also acts as a depressor. Needle position: One centimeter lateral to the midpoint between the inferior surface of the symphysis of the mandible and the body of the hyoid bone. Introduce the needle 45° obliquely over the transverse plane in the anteroposterior direction. Morphology: Wide muscle with parallel fibers. Depth: 2.5–3 cm

M. Crycothyroid (Picture 3.11) Origin: Anterolateral portion of the cricoid cartilage Insertion: inferior margin of the thyroid cartilage Innervation: superior laryngeal nerve Action: pulls the thyroid cartilage anteriorly and inferiorly, tensioning the vocal folds (high-pitched sounds). Active electrode: palpate the space between the lower margin of the thyroid cartilage and the upper margin of the cricoid. Insert 2 cm from the midline between the two margins directing the needle 45° externally. Morphology: Short with oblique fibers. Depth: 1.5 cm.

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M. Temporalis (Picture 3.12) Origin: External face of the temporal bone and fascia. Insertion: Anterior border and medial face of the mandibular coronoid process. Innervation: Trigeminal nerve (V cranial pair). Action: Elevation (occlusion) and retraction of the mandible. Active electrode: Midpoint of the temporal fossa. Morphology: Wide muscle with parallel fibers. Depth: 1.5 cm

M. masseter (Picture 3.13) Origin: Inferior margin of the zygomatic bone and zygomatic arch. Insertion: Lateral face of the mandibular angle. Innervation: Trigeminal nerve (V cranial pair). Action: Elevation (occlusion) of the mandible. Active electrode: Two to three centimeters anterior to the mandibular angle. Morphology: Wide muscle with parallel fibers. Depth: 1.0–1.5 cm

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M. Sternocleidomastoid (Picture 3.14) Origin Clavicular head: medial third of the superior surface of the clavicle. Sternal head: anterior face of the sternal notch and sternoclavicular joint. Insertion: Lateral third of the superior nuchal line and mastoid process of the temporal bone. Innervation: Accessory nerve (XI cranial pair) and cervical plexus (C1-C2-C3). Action: On unilateral contraction it rotates the head to the opposite side and can also, at the same time, flex it to the same side. On contraction of both muscles, the head is stretched and pulled anteriorly. Active electrode: midpoint between mastoid process and the jugular notch of the sternal bone. Morphology: Long muscle, with two main heads and parallel fibers. Depth: 0,5–1 cm

M. trapezius (Picture 3.15) Origin: External occipital protuberance and spinous processes of C1 to C7 Insertion: Lateral third of clavicle Innervation:: Accessory nerve and motor branches of C2, C3, and C4 Action: Mainly shoulder elevation Active electrode: Midpoint between the acromion and the occipital region Morphology: Wide Depth: 1.5–2.5 cm

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M. supraespinatus (Picture 3.16) Origin: Supraspinatus fossa of scapula Insertion: Greater tubercle of humerus Innervation: Suprascapular nerve (C5, C6) Action: Arm abduction Active electrode: Midpoint of its belly. For most appropriate recording recommended insulated and long needles to isolate from more superficial trapezius muscle. Morphology: Fusiforme Depth: 3–4 cm

M. infraspinatus (Picture 3.17) Origin: Supraspinatus fossa of scapula Insertion: Greater tubercle of humerus Innervation: suprascapular nerve (C5, C6) Action: External rotation Active electrode: Half of an imaginary line between the midpoint of the scapular spine and its inferior angle. For the same reason as the supraspinalis, insulated long needles are recommended. Morphology: Oblique and multipenate Depth: 2 cm

M. Deltoid (Picture 3.18) Origin: Acromion Insertion: Humerus Innervation: Axillary nerve (C5, C6) Action: Abduction Active electrode: Midpoint of its medial segment Morphology: Oblique and multipenate Depth: 1–2 cm

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M. Biceps brachii (Picture 3.19) Origin Short head: coracoid process of the scapula Long head: supraglenoid supraglenoidal tubercle of the scapula Insertion: radius tuberosity Innervation: Musculocutaneous nerve (C5, C6) Action: Supination of the forearm and flexion of the upper arm. Active electrode: Midpoint of the anterior segment of the arm Morphology: Parallel and fusiform Depth: 2 cm

M. triceps brachii (long head) (Picture 3.20) Origin: Infraglenoid tubercle of the scapula Insertion: Olecranon Innervation: Radial nerve (C6, C7, C8) Action: Extension of the forearm Active electrode: Distal third of the posterior portion of the humerus Morphology: Parallel Depth: 1.5 cm

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M. extensor carpi radialis (Picture 3.21) Origin: Lateral supraepichondylar crest of the humerus Insertion: Base of the 2nd metacarpal Innervation: Radial nerve (C6, C7) Action: Extension and radial deviation of the hand Active electrode: 2 cm distal to the lateral epicondyle. Morphology: Long Depth: 1–2 cm

M. extensor digitorum (Picture 3.22) Origin: Lateral epicondyle of the humerus Insertion: Extensor expansions of the four fingers Innervation: Radial nerve (C7, C8) Action: Extension of the fingers Active electrode: the extensor digitorum is the second muscle belly laterally to the brachioradialis in the proximal third of the forearm. Morphology: Long Depth: 1 cm

M. brachiorradialis (Picture 3.23)

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Origin: Supracondylar process of humerus Insertion: Distal extremity of the radius Innervation: Radial nerve (C5, C6) Action: Flexion of the forearm in neutral position Active electrode: With the forearm flexed and in neutral position, the muscle is in its proximal third. Morphology: Parallel Depth: 2 cm

M. pronator teres (Picture 3.24) Origin: Coronoid process and medial epicondyle of humerus Insertion: Proximal lateral face of the radius Innervation: Median nerve (C6, C7) Action: Pronation of the forearm Active electrode: Palpate the medial border of the biceps tendon and draw a line from this point to the medial epicondyle. At the midpoint of this imaginary line, descend three fingers distally. Morphology: Short and longitudinal Depth: 1–1.5 cm

M. flexor carpi radialis (Picture 3.25) Origin: Medial epicondyle of the humerus Insertion: Base of the 2nd metacarpal Innervation: Median nerve (C6, C7) Action: Flexion and radial deviation of the hand Active electrode: Identify the tendon of the flexor carpi radialis at the wrist and follow proximally to the myotendinous transition (point where it is more difficult to palpate the tendon). At this point, draw an imaginary line to the medial epicondyle. The muscle is at the midpoint of this line. Morphology: Long and bipenate Depth: 1 cm

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M. flexor carpi ulnaris (Picture 3.26) Origin: Medial epicondyle of the humerus Insertion: Pisiform, hamate, and 5th metacarpal Innervation: Ulnar nerve (C8, T1) Action: Flexion and ulnar deviation of the hand Active electrode: Identify the tendon of the flexor carpi ulnaris at the wrist the wrist and follow proximally to the myotendinous transition (point where it becomes more difficult to palpate of the tendon). At this point, draw an imaginary line to the medial epicondyle. The muscle is located at the midpoint of this line. Morphology: Long and fusiform Depth: 1–2 cm

M. extensor indicis (Picture 3.27) Origin: Distal third of the ulna Insertion: Expansion of the extensor muscle of the 2nd finger Innervation: Radial nerve (C7, C8) Action: Extension of the index finger Active electrode: With the hand in pronation, the muscle is three fingerbreadths above the styloid process of the ulna. Morphology: Long Depth: 0.5

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M. Abductor pollicis brevis (Picture 3.28) Origin: Retinaculum of flexors Insertion: Lateral face of the 1st metacarpal Innervation: Median nerve Action: Abduction of the thumb (C8, T1) Active electrode: Midpoint of the 1st metacarpal bone, close to the medial edge of the bone. Morphology: Short Depth: 0.5 cm

M. abdutor digiti minimi (Picture 3.29) Origin: Pisiform Insertion: Base of the proximal phalanx of the minimum finger Innervation: Ulnar nerve Action: Little finger abduction (C8, T1) Active electrode: On the medial border, midpoint of the 5th metacarpal Morphology: Short and fusiform Depth: 0.5 cm

M. diaphragm (Picture 3.30) Origin: Internal surfaces of lower costal cartilages na ribs 7–12 Insertion: Central tendon of diaphragm Innervation: Nervo frênico (C3, C4, C5) Action: Primary muscle of breathing (inspiration) Active electrode: At the anterior axillary line superior to the 9th or 10th rib. Ultrasound Image Guidance Is recommended. Morphology: Large muscle with radial fibers Depth:

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M. obliquus abdominis (Picture 3.31) Origin: External surfaces of ribs 5–12 Insertion: Linha Alba, pubic tubercle and anterior half of iliac crest Innervation: Intercostal nerves (T7-T11) and subcostal nerve (T12) Action: ipsilateral trunk lateral flection, contralateral trunk rotation, and trunk flection (bilateral contraction) Active electrode: Halfway between linea alba and midaxillary line. Morphology: Large with oblique fibers Depth: 1,5–2 cm 1, cm

M. intercostalis (Picture 3.32) Origin: Costal groove of ribs Insertion: Superior border Innervation: Intercostal nerve Action: Depress ribs during forced expiration Active electrode: Half way between costocondral articulations and axilary line. Morphology: Short with oblique fibers Depth:

M. Rectus abdominais (Picture 3.33) Origin: Pubic Symphysis Insertion: Xiphoid process and costal cartilages of ribs 5–7 Innervation: Ictecostal nerves (T7-T11) and subcostal nerve (T12) Active electrode: 10 points disposed 5 cm from the midline. Depth: 2–3 cm

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M. iliacus (Picture 3.34) Origin: Iliac crest, iliac fossa, and sacral wing Insertion: Psoas major and lesser trochanter Innervation: Femoral nerve (L2, L3) Action: Flexion of the thigh Active electrode: Midpoint between the anterosuperior iliac spine and the femoral artery, directly below the inguinal ligament (tilt the needle 45° toward the internal face of the iliac bone). Morphology: Wide Depth: 5–9 cm

M. adductor longus (Picture 3.35) Origin: Body of pubis Insertion: Middle third of femur Innervation: Obturator nerve (L2, L3, L4) Action: Adduction of the thigh Active electrode: Proximal third of the medial aspect of the thigh Morphology: Wide Depth: 2–4 cm

M. Addcutor brevis (Picture 3.36) Origin: Body of pubis Insertion: Pectineal line Innervation: Obturator nerve (L2, L3) Action: Adduction of the thigh Active electrode: Proximal third of the medial aspect of the thigh Morphology: Wide and longitudinal Depth: 2–4 cm

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M. rectus femoris (Picture 3.37) Origin: Anteroinferior iliac spine Insertion: Tibial tuberosity Innervation: Femoral nerve (L2, L3, L4) Action: Knee extension, flexion of the thigh Active electrode: Midpoint between anterosuperior iliac spine and the superior border of the patella. Morphology: unipenate Depth: 1–2 cm (from 3 cm depth on, the vastus muscle the vastus intermedius)

M. tibialis anterior (Picture 3.38) Origin: Lateral condyle of the tibia Insertion: Medial cuneiform and base of 1st metatarsal Innervation: Deep peroneal nerve (L4, L5) Action: Dorsiflexion and inversion of the foot Active electrode: Proximal third of the tibia, 1 cm lateral to its anterior margin. Morphology: long and with parallel fibers Depth: 1 cm

M. extensor hallucis longus (Picture 3.39) Origin: Anterior face of the fibula and interosseous membrane Insertion: Base of the distal phalanx of the hallux Innervation: Deep peroneal nerve (L5, S1) Action: Hallux extension Active electrode: Four to five toes and 1 cm lateral to the midpoint of the bimalleolar line. Morphology: Oblique and bipennate Depth: 1–2 cm

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M. gastrocnemius (Picture 3.40) Origin Lateral head: Lateral condyle of the femur Medial head: Medial condyle of the femur Insertion: Posterior surface of the calcaneus Innervation: Tibial nerve (S1-S2) Action: Mainly plantar flexion Active electrode: Upper third of the posterior aspect of the leg (lateral head in the lateral portion and medial head in the medial portion). Obs: By performing digit pressure on the lower part of the popliteal fossa fossa, two protrusions (medial and lateral gastrocnemius) are observed that correspond to the motor points of the portions of this muscle. Morphology: Oblique and bipennate Depth: 2–3 cm

M. Abductor hallucis (Picture 3.41) Origin: Medial process of calcaneal tuberosity and plantar aponeurosis Insertion: Proximal phalanx of great toe Innervation: Medial plantar nerve (S1-S2) Action: Toe abduction and flexion Active electrode: 2 points are possible. In the proximal third of metatarsus and 2 fingerbreadths below and anterior to talus bone. Morphology: Long with oblique fibers Depth: 1–1.5 cm.

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M. gluteus maximus (Picture 3.42) Origin: Ilium posterior to the posterior gluteal line, dorsal aspect of the sacrum and coccyx Insertion iliotibial tract Innervation: Inferior gluteal nerve (L5, S1, S2) Action: Extension of the thigh Active electrode: Four fingerbreadths inferiorly to the posterior most prominent posterior portion of iliac crest, insert the needle obliquely toward the greater trochanter Morphology: Large and oblique Depth: 3 cm

M. gluteus medius (Picture 3.43) Origin: External face of the ilium Insertion: Femoral greater trochanter Innervation: Upper gluteal nerve (L5, S1) Action: Abduction and medial rotation of the thigh Active electrode: Two centimeters inferior to the anterior third of the iliac crest Morphology: Oblique Depth: 3 cm

Gluteus minimus (Picture 3.44) Origin: External face of the ilium Insertion: Femoral greater trochanter Innervation: Upper gluteal nerve (L5, S1) Action: Medial rotation of the thigh Active electrode: Midpoint between greater trochanter femoris and the midline posterior border of the iliac crest. Morphology: Oblique Depth: 3–4 cm

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M. semitendinosus (Picture 3.45) Origin: ischial tubercle Insertion: Upper part of the medial aspect of the tibia (tibial plateau) Innervation: Tibial division of the sciatic nerve (L5, S1, S2) Action: Hip extension, flexion, and internal rotation of the leg Active electrode: Midpoint between tuber ischium and medial tibial plateau. Displace 2 cm lateral. Morphology: Parallel Depth: 2.5–4 cm

M. Semimembranosus (Picture 3.46) Origin: ischial tubercle Insertion: Upper part of the medial aspect of the tibia (tibial plateau) Innervation: Tibial division of the sciatic nerve (L5, S1, S2) Action: Hip extension, flexion, and internal rotation of the leg Active electrode: Midpoint between ischial tubercle and medial tibial plateau. Morphology: Parallel Depth: 2.5–4 cm

M. bíceps femoris – long head (Picture 3.47) Origin: ischial tuber Insertion: Fibula head Innervation: Tibial portion of the sciatic nerve (L5, S1, S2) Action: Hip extension, flexion, and external rotation of the leg Active electrode: Midpoint between the ischial tubercle and fibular head. Morphology: Oblique Depth: 2.5–4 cm

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M. biceps femoris- short head (Picture 3.48) Origin: Lateral supracondylar line of the femur Insertion: Fibula head (L5, S1, S2) Innervation: Common fibular division of the sciatic nerve Action: Hip extension, flexion, and external rotation of the leg Active electrode: Distal third between the ischial tubercle and fibular head. Morphology: Oblique Depth: 2.5–4 cm

M. tensor fasciae latae (Picture 3.49) Origin: Anterosuperior iliac spine Insertion: Lateral condyle of the tibia Innervation: Upper gluteal nerve (L4, L5, S1) Action: Abduction and medial rotation of the thigh Active electrode: Two fingers medially to the greater trochanter Morphology: Parallel Depth: 2 cm

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M. perineal transversus (deep and superficial portions) (Picture 3.50) Origin: Inferior rami of the ischium Insertion: Deep transverse perineal muscle of the opposite side Innervation: Pudendal nerve Action: Constricts urethra and vagina Active electrode in women: 2 ponts 3 cm away from midline lateral to vaginal introitus, just between midline and ischium. Active electrode in men: Halfway between ischial tuberosity and pênis crus just between middle line and ischium. Morphology: Large with parallel fibers Depth: 3 cm

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M. Ischiocavernosus (Picture 3.51) Origin: Ischial tuberosity and ramus Insertion: crus of clitoris or penis Innervation: Deep branch of pudendal nerve (S2-S4) Action: Maintains erection of penis/clitóris, pushes blood from root to body of clitóris/penis Active electrode: Halfway between the ischial tuberosity and penis/clitoris crus just medial to ischium. Morphology: long with parallel fibers Depth: 2 cm

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M. Bulboespongiosus (Picture 3.52) Origin: Perineal body, median penile raphe Insertion: Pubic arch, fascia of corpora cavernosa and clitoris (female). Perineal membrane, fascia of vulv of penis, and dorsal aspect of corpus spongiosum. Innervation: Deep branch of pudendal nerve Action: Assists in erection of clitóris/pênis, supports perineal body Active electrode in men: 4 points 2 cm away from the midline between testicle and anal sphincter. Active electrode in women: Halfway between external urethral sphincter and vaginal introitus, 2 cm from the midline. Morphology: n/s Depth: 2 cm

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M. external urethral sphincter (Picture 3.53) Origin and insertion: encircles membranous urethra Innervation: Deep branch of pudendal nerve Action: Maintains urinary continence and prevents retrograde ejaculation Active electrode: 2 points 1 cm away from the external urethral orifice (just in women). Morphology: sphincter Depth: 2 cm

M. internal anal sphincter (Picture 3.54) Origin and insertion: surrounds the upper 2/3 of the anal canal. Innervation: Inferior anal/rectal branch of pudendal nerve (S2-S4) Action: Fecal continence Active electrode: 2 points 1 cm away from the anal orifice. Morphology: sphincter Depth: 2, 5 cm

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M. external anal sphincter (Picture 3.55) Origin: Skin and fascia around anus Insertion: Perineal body and anococcygeal ligament Innervation: Inferior anal/ rectal branch of pudendal nerve (S2–S4) Action: Constricts anal canal and supports pelvic floor Active electrode: 4 points in a radial fashion 3 cm away from the anal orifice in each of 4 quadrants. Insert neele in a 45° direction towards the anal orifice. Morphology: sphincter Depth: 1 cm

References 1. Botter A, Oprandi G, Lanfranco F, Allasia S, Maffiuletti NA, Minetto MA. Atlas of the muscle motor points for the lower limb: implications for electrical stimulation procedures and electrode positioning. Eur J Appl Physiol. 2011;111(10):2461–71. https://doi.org/10.1007/ s00421-­011-­2093-­y. PMID: 21796408. 2. Christensen E. Topography of terminal motor innervation in striated muscles from stillborn infants. Am J Phys Med. 1959;38(2):65–78. PMID: 13637190. 3. Chu J, Chan RC, Bruyninckx F.  Progressive teflon denudation of the monopolar needle: effects on motor unit potential parameters. Arch Phys Med Rehabil. 1987;68(1):36–40. PMID: 3800622. 4. Coers C, Durand J. La répartition des appareils cholinestérasiques en cupule dans divers muscles striés [Distribution of cup-shaped cholinesterase apparatus in various striated muscles]. Arch Biol (Liege). 1957;68(2):209–15. French. PMID: 13445292. 5. Dong CCJ, MacDonald DB, Akagami R, Westerberg B, AlKhani A, Kanaan I, Hassounah M. Intraoperative facial motor evoked potential monitoring with transcranial electrical stimulation during skull base surgery. Clin Neurophysiol. 2005;116(3):588–96. 6. Dumitru D, Zwarts MJ, Amato AA, editors. Elctrodiagnostic medicine. 2nd ed. Elsevier; 2002. 7. Feinstein B, Lindegard B, Nyman E, Wohlfart G. Morphologic studies of motor units in normal human muscles. Acta Anat (Basel). 1955;23(2):127–42. https://doi.org/10.1159/000140989. PMID: 14349537.

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8. Gobbo M, Gaffurini P, Bissolotti L, Esposito F, Orizio C.  Transcutaneous neuromuscular electrical stimulation: influence of electrode positioning and stimulus amplitude settings on muscle response. Eur J Appl Physiol. 2011;111(10):2451–9. https://doi.org/10.1007/ s00421-­011-­2047-­4. PMID: 21717122. 9. Gobbo M, Maffiuletti NA, Orizio C, Minetto MA. Muscle motor point identification is essential for optimizing neuromuscular electrical stimulation use. J Neuroeng Rehabil. 2014;25(11):17. https://doi.org/10.1186/1743-­0003-­11-­17. PMID: 24568180; PMCID: PMC3938308. 10. Jabre JF. Concentric macro electromyography. Muscle Nerve. 1991;14(9):820–5. https://doi. org/10.1002/mus.880140904. PMID: 1922175. 11. Jahangiri FR, Trausch C. Utilizing longer intramuscular needle pair electrodes: what are we missing in our intraoperative muscle recordings? EC Neurol. 2019;11(4):288–94. 12. Kim DH, Zaremski J, Kwon B, Jenis L, Woodard E, Bode R, Banco RJ.  Risk factors for false positive transcranial motor evoked potential monitoring alerts during surgical treatment of cervical myelopathy. Spine (Phila Pa 1976). 2007;32(26):3041–6. https://doi.org/10.1097/ BRS.0b013e31815d0072. PMID: 18091499. 13. AAEE glossary of terms in clinical electromyography. Muscle Nerve. 1987;10(8 Suppl):G1–60. PMID: 3657851. 14. Polgar J, Johnson MA, Weightman D, Appleton D.  Data on fibre size in thirty-six human muscles. An autopsy study. J Neurol Sci. 1973;19(3):307–18. https://doi. org/10.1016/0022-­510x(73)90094-­4. PMID: 4716847. 15. Skinner SA, Transfeldt EE, Savik K. Surface electrodes are not sufficient to detect neurotonic discharges: observations in a porcine model and clinical review of deltoid electromyographic monitoring using multiple electrodes. J Clin Monit Comput. 2008;22(2):131–9. https://doi. org/10.1007/s10877-­008-­9114-­3. PMID: 18335318. 16. Stålberg E.  Macro EMG, a new recording technique. J Neurol Neurosurg Psychiatry. 1980;43(6):475–82. https://doi.org/10.1136/jnnp.43.6.475. PMID: 7205288; PMCID: PMC490586. 17. Stålberg E, Antoni L. Electrophysiological cross section of the motor unit. J Neurol Neurosurg Psychiatry. 1980;43(6):469–74. https://doi.org/10.1136/jnnp.43.6.469. PMID: 7205287; PMCID: PMC490585. 18. Van Campenhout A, Molenaers G. Localization of the motor endplate zone in human skeletal muscles of the lower limb: anatomical guidelines for injection with botulinum toxin. Dev Med Child Neurol. 2011;53(2):108–19. https://doi.org/10.1111/j.1469-­8749.2010.03816.x. PMID: 20964675.

Chapter 4

Safety and Troubleshooting Jose Alberto Nunes Sobrinho, Monica Nascimento de Melo, and Silvia Mazzali Verst

Abbreviations DCS DBS EEG EMG EP IOM OR MEP TES SSEP

direct cortical stimulation deep brain stimulator electroencephalography electroneuromyography evoked potentials intraoperative monitoring operating room motor evoked potential transcranial electrical stimulation somatosensory evoked potential

Supplementary Information The online version contains supplementary material available at [https://doi.org/10.1007/978-­3-­030-­95730-­8_4]. J. A. Nunes Sobrinho (*) Department of Neurophysiology, Stela Clinic, Brasilia, Brazil M. N. de Melo Department of Neurophysiology, Integrated Neuroscience Institute, Goiânia, GO, Brazil S. M. Verst Instituto de Ensino e Pesquisa (Research and Educational Institute) of Sírio Libanês Hospital, São Paulo, Brazil Brain Spine Neurofisiologia, Jundiaí, SP, Brazil © The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 S. M. Verst et al. (eds.), Intraoperative Monitoring, https://doi.org/10.1007/978-3-030-95730-8_4

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Introduction IOM advances as a medical specialty that combines neurological signals analysis in real-time with surgical approaches. Integration of multimodal analysis offers a better understanding of neurological reactions, enhancing surgeon’s maneuvers to avoid neural damage. The modalities of evoked potentials (EP), electroneuromyography (EMG), and electroencephalography (EEG) are interspersed as frequently as possible since simultaneity is neither desired nor possible. As the sophistication of neurophysiological signal modalities ensues, it is paramount to hasten the development of systems that safely stimulate and record, without posing a hazard to the patient’s integrity. Neurophysiological practice involves the interaction of two large electrical systems: the human body and a recording machine. Both are sources of electric current generation, energy dissipation, resistance to transmission, charge storage, and production of electric and magnetic vectors, and, as such, are subject to the same physical laws. The dynamics of electrical interaction and induction of magnetic fields created by electron displacement establish the basic notions for obtaining the most appropriate recordings [1–3]. It reduces interference as well as enhances the electrical safety of the patient and examiner, thus preventing injuries. The direct effect of the electric current on the corticospinal tract produces physical effects on the body such as movements with possible biting of the tongue and lips, seizures, and arrhythmia. The use of invasive electrodes such as needles, cortical grids, and spinal electrodes increases the risk of infection and bleeding. It is paramount for good practice that the neurophysiologist predicts these risks and minimizes them whenever possible. In the OR numerous electrical devices are simultaneously and competitively connected to or close to the patient, like mechanical ventilators, catheters, infusers, body warmers, electrosurgical devices, cardioverters, neuronavigators, aspirators, lamps, and cleaning devices. All these connections increase both the presence of artifacts and electrical noise in the IOM recordings, and the electrical risk to which the patient is exposed. The catastrophic event occurs when an amount of current, over the estimated, enters the body, and/or follows the flow to exit via an unexpected route. Therefore, for better prevention and minimization of risks, the knowledge of the basic elements of physics and its application becomes primordial.

Physics Applied to Neurophysiology The displacement of the electrons follows the principle of energy saving, starting from the largest orbit to the least energy orbit, and is titled electric current (i) to its flow during the time, whose vector representation has opposite direction to the movement. As a result, we have as fundamental concept that the electric current is

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directly proportional to the amounts of charges (Q) that moves during a unit of time in which the movement (t) occurs, deducting the formula below:

i =Q/t

where current is measured in Amp (A) and represents the charge of 1 Coulomb (C) in 1 second. The ease of losing or gaining electrons determines the conductivity of the material (conductive and non-conductive), and the more uniform its composition, the more predictable its behavior will be. For example, consider the differences in pedicle screw composition and the impact it results in determining threshold values (see Chap. 23 for details). To generate the current, it is necessary to establish a difference in charges between two points (in neurophysiology, two electrodes), since equilibrium is assumed as the natural state. Without this maintenance of the differential, the tendency of electrons is to occupy their orbits of stable movements tending to neutrality.

Concepts Applied to IOM Electrical Current and Charges The favorable property of materials for displacement of loads depends on their structure, giving their nature to be conductive or non-conductive. The easier the electrons pass through the material, the lower its resistivity or electrical resistance, and the greater its conductivity. Conversely, the more difficult the displacement, the greater resistivity, less conductivity, and more suitable for charges storage is the material in question. It can be anticipated that non-conductive materials are used in the production of capacitors for charge storage (see below), and mixed compounds that use different materials can function both as conductor and as storage according to the predominant characteristic in a particular situation, as in the case of the human body. Important concepts reflected in electrical safety are established: (a) The higher the voltage of the electrical source (V), the greater the amount of current (i) generated by the greater amount of charge (Q) in motion (b) Joules’ Law (James P. Joules, 1849): the heat/energy raised by the passage of the electric current is proportional to the conductor’s resistance, to the square of the voltage intensity, and to the time during which it passes in the conductor. If only the relationship among voltage and current is considered, regardless of time, we arrive at the definition of work (T, in watt). The kinetic energy of the electron movement correlates the work directly proportional to the amount of charge (Q) and the voltage that prints this displacement (V) over time (in joules).

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Thus,

Τ = V ×i



E = V ×Q∴E = V ×i × t

what enables us to accurately predict that higher the voltage or current, and longer the time involved, more energy or heat will be produced. Consequently, it is greater the risk of burns. Classic consequences of electric current flow through the body include direct effects on cell membranes (e.g., cellular depolarization or electroporation), at nerve and muscle cells, burns and deep necrosis (in alternating current accidents) [4]. However, brain damage and kindling are highly unlikely [5]. Electric currents can be either alternated or pulsed, in consonance to the variation over time, defining the shape of the wave (square, triangular, sinusoidal, exponential, etc.), and according to the direction that the charges move (single-phase or two-phase). According to international conventions and safety parameters, IOM equipment uses low voltage direct current (4). Regarding biphasic waves, they can have equal (symmetrical) or different (asymmetric) amplitudes. The duration or width of the pulse (D) determines the duration of time that the charges will pass on each pulse. Altogether, taking a square wave as an example, the total charge dispensed will depend on the current intensity, the pulse duration, the number of pulses, and the wave morphology

Qt = i × D × Npulse (×2,if biphasic )



If the wave is sinusoidal, it is corrected with a factor of 0.637; if the current has an exponential decay (charge generated by a capacitor), it is multiplied by the time constant related to the discharge [6]. Caution with electrical safety is an important step in IOM protocols and the stimulus parameters cannot be set randomly. The amount of charge delivered is a product of Intensity x Pulse Duration x Stimulator Electrode Diameter (Coulomb’s Law). Electrode diameter is directly responsible for charge density. Resistance, Impedance, and Reactance One must ponder the resistance (R, measured in Ω), whose usefulness is to disperse the kinetic energy of electron movement in heat. If there was no interposition of this element, the amount of energy that would reach the poles of the source would quickly destroy them. At this point it is worth remembering two significant laws, namely: I. Ohm’s Law (Georg S. Ohm, 1826): voltage results from the product of resistance versus current. If we have a constant resistance, the electric current will be proportional to the system voltage. On the other hand, the greater the resistance of the material, the lower the current.

V = R × i ∴i = V / R

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In a circuit where the resistors are arranged in a series system, the total resistance will be the direct sum of the resistances. According to Ohm’s law, in a constant voltage stimulator the delivered charge will not overcome tissue resistance variation and can be lower of the established. Conversely, by a constant current stimulator, the final charge will be established since it will adapt to tissue resistance. This directly impacts many tests in IOM. Taking as an example TES for corticobulbar tract, if there is a variation due to scalp edema or air inside the skull, the final delivered current may be not enough for supramaximal activation of the motor pathway (more details in Chap. 21). II. Kirchhoff’s Laws (Gustav Kirchhoff, 1845): the energy in one system can be transformed into another, but its total will be the sum of the values ​​(general law of energy conservation). The same is true about the current: the total current entering a node in the closed system will be equal to the sum of the leaving currents. Likewise, the voltage in a mesh system of that node will be the same for all devices. Therefore, in a parallel system, the sum of the resistances will be represented by its inverse, according to the formula below

it = i1 + i 2 …∴ V / Rt = V / R1 + V / R 2 …



or, simplifying V ,



1 / Rt = 1 / R1 + 1 / R 2 …

Energy can also be defined as the function among voltage, electric current, charge, and resistance, established by Joules’ law combined with Ohms’ law. Thus, we will have the formulas:

E = i ^ 2 × t × R ∴ E = V ^ 2 / R × t ∴ E = i ^ 2 × D × R,

where time is replaced by the duration of the stimulus to determine the total charge. However, we must consider the equivalent resistance applied to the neurophysiological routine. There will be both resistances from different equipment in parallel connected to the patient and the human body also acting as another equivalent total resistance in parallel (resulting from the sum of several “resistances” in series of the different tissues). The calculation is not an easy task since body resistance is not stable. It depends on many factors that are neither accessible nor controllable, such as the dynamic variation of the body reacting to the variation in volume of the instilled fluids, organic composition, stature, size, and thickness of the organs, to mention some examples. Being this the case, in an equipment composed of several electrical elements constituted of different materials, it is not appropriate to call it resistivity and resistance, which is the peculiar property of each of them, but impedance (Z), measured in Ω), the same relationship remaining in accordance with Ohms’ law. Example: a copper resistor has its resistivity and resistance checked by the material of the alloy that composes it, and it is perfectly calculated. However, equipment resistance is not

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spoken when several compound electronic components are integrated and made of different materials, but, instead, impedance. Although the impedance translation is mistaken for the “resistance” to the electrical passage, it goes beyond the characteristic heat dissipation nature and includes the storage of electrical charges and energy (capacitance), and the reason for the associated magnetic flux that passes through the circuit (inductance). The combination of these properties determines reactance (X) of the system. The same situation is applied to the human body, which offers a variable reactance according to its individual composition, able to accumulate charges, dissipate, transfer, and induce currents according to its variable composition, its physical-chemical state, and according to its content.

Z = R+X

The risks arising from elements of low resistance arranged on the surface or inside the human body, such as catheters, metal electrodes, or wires, appear to be more understandable, making it easier to drain incoming or accumulated charges. The human body itself has areas of greater or lesser conductivity, and depending on the physiological state, presenting greater or lesser reactance. The arrangement of tissues makes the human body a semiconductor system with heterogeneous charge storage capacity, making its reactance fluctuate constantly. As the dry skin, dermis, tendons, and bones offer greater impedance, damp skin, muscles, nerves, and the bloodstream behave in the exact opposite manner. Following the same line of reasoning, the conditions surrounding the body favor the reduction of impedance, such as wet surfaces or even their immersion in water or contact with conductive or non-conductive materials. Considering IOM practice, the insertion of catheters, subdermal or intramuscular electrodes, plates, surface electrodes with conductive gel, among several others, are favorable means for the transmission of charges, and are sometimes more relevant due to the decrease in reactance [7]. Recalling, electric displacement obeys the rule of energy saving: where there is less impedance, less resistivity, less difficulty to flow, and greater conductivity, this will be the path of choice for the stream of electron flow [2]. Capacitor and Filters The charge rate of the capacitor depends on the variation of the voltage of the source for the accumulation of charges, and the current generated by its discharge depends on the frequency of variation of the voltage of the source, both following an exponential relationship with the time constant. A practical importance regarding the study of the system’s capacitance is found in the generation of electrical artifacts: the lower this property of the device, the greater the chance that the current generated by the system source reaches electrodes and causes electrical artifacts [8, 9]. The neurophysiology device combines resistance and capacitor connected to the same source, that is, one element that disperses and another that accumulates energy. This alliance between antagonistic elements allows modulation in

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obtaining signals, where the restriction of high frequencies and the passage of low frequencies correspond to the capacitive property of the system, while the inverse takes place when it comes to the resistance. The time constant, which is directly proportional to capacitance and resistance, and represents the time for the current to charge the capacitor could be compared to the width of a narrow gap: the wider, the greater the composition of slow frequencies, and the narrower, the greater the composition of fast frequencies. The high- and low-frequency filters consist of the parallel association of the resistor or the capacitor, whose determination of which of the two is connected in series with the source will define which type of frequency will have its passage restricted. To provide a better understanding of the process, we return to the capacitor reactance concept (XC) to establish the relationship with the frequency of the waves (f) using the formula below:

Xc = 1 / 2π fC

C is the capacitance (invariant constant) of the capacitor. We can predict that higher frequencies will produce lower reactance X and this will make it harder for low-frequency waves to pass, and consequently lower frequencies will determine higher reactance X, which will offer a barrier to the passage of higher frequencies. If the capacitor is connected in series with the power source, it will prevent low frequencies from passing and will favor the passage of high frequencies (low-­ frequency filter). If the capacitor is connected in parallel with the source, the low frequencies will not be restricted to the passage, but the resistance connected in series will hinder the passage of the high frequencies. Defining the resistance value, we will restrict the cut of the high frequency that we want (high-frequency filter). This cutoff frequency is defined as the value that will produce the attenuation of 30% of the input value, which corresponds to equal values ​​of the reactance and the capacitance (R = XC). In high-frequency filters, values ​​above the stipulated cutoff frequency are attenuated by 70%, while in low-frequency filters the reverse occurs (frequencies below the cutoff value will be reduced by 70%). Filtering is an important issue regarding IOM success. Since there is a direct influence between the filter band and the potential amplitude, the narrower the band, the smaller the amounts of axons visualized within the potential. For practical purposes, the arrangement of the capacitor in series with the source defines the low-frequency filter, and the capacitor in parallel with the source specifies the high-frequency filter, whose cut will be determined by the resistance. Grounding in IOM It is fundamental to ensure that unwanted or unforeseen currents do not circulate through patient’s body, since it can trigger catastrophic or unpleasant events. To avoid risks, it is imperative to eliminate these charges out of the circuit by draining through grounding. Its primary function is to offer a safe path to eliminate this energy, protecting the system from damage (both the equipment and the individual

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connected to it). The ideal ground is one that offers low resistance, high conductivity, and dispersion of charges (guarantee of low density of charges), while remaining neutral. Although this ideal element does not exist in the practical reality, the Earth represents the closest thing that can be reached due to its characteristics (mass dimension and distribution of charges over its surface, resulting in low density, added to the equipotential distance given by the radius of the planet). By extension, any electrical element that favors the dispersion of charges is called ground, although this nomination might produce confusion in certain circumstances. The ground of the electrical network to which the ground of the device box (chassis) is connected (for the dispersion of charges to the Earth) is not the same for “patient ground” (for dispersion of charge from the recording electrodes). Patient’s ground is related to impedances measurement to reduce artifacts at the registration site [10, 11]. It represents the establishment of a point of comparison between differential amplifiers to reject signals in common mode and are arranged electronically isolated from all other grounds. Meanwhile, the electrical network ground (true ground) consists of the electrical component for draining the current, even that produced by the magnetic induction generated by the circulation of electrons in the electrical components (leakage currents). Exceptionally, in anomalous conditions of true ground operation, flow of electrical charges through this route offers a high risk of an overload to the patient and the system. Hence pronounced attention ought to be paid to the conditions of the ground. The protection recommendations require the existence of effective grounding of the devices, and this must not be the neutral pole of the power line. It is recommended not adding more than one ground to the patient to avoid loop current formation between both points (Fig.  4.1). All electrical equipment connected to the patient must be connected to the same set of sockets to ensure the same equipotential ground (Fig.  4.2). It is recommended never to use devices other than medical/hospital devices in the same network system to which the patient is connected. The reason is that non-electronic biomedical devices can have leakage current greater than the determined safety limit [10, 11]. In conditions of malfunction of the device, the generation of leakage current can have its draining flow interrupted in the presence of a ground break. It could be any of the system’s ground: the internal ground cable of the device connected to the chassis, the ground of the cable of the voltage cable, or the ground system of the electrical network. Under these conditions, the generated charge may use another route of less reactance to escape, passing through the electrodes and going to the patient. For safety reasons, the exhaust current is set below 100μV or 100μA for medical and electronic medical devices in normal conditions (and 500μA for the patient when not connected to devices). Intensity of 20μV or 10μA, if applied directly to the endocardium or to smaller individuals, can generate ventricular fibrillation [6, 10]. Bearing in mind the risks of electrical current passing through the myocardium and subsequent severe and symptomatic arrhythmia, the International

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EEG ground

EEG

EKG CCF EKG ground

© 1999

Fig. 4.1  Non-equipotential grounds. The magnetic field generated by the power wiring induces current into ground loop. If, due to the positioning of the cables of the different equipment, the patient becomes a conducting part of this loop and conducts the current, an injury can occur. (From Levin KH, Luders HO (2000). Comprehensive Clinical Neurophysiology, WB Saunders)

Electrotechnical Commission establishes the heart current factor as the ratio of the risk of rhythm disturbance and cardiac conduction (the most deleterious being ventricular fibrillation) compared to the passage of current through the left hand and foot (F = 1) according to possible pathways (Table 4.1) [6]. The awareness of this notion enables the proposal of the strategy of placing the grounding plates on the patient’s body according to the lowest values of ​​ F, minimizing the severity in unwanted events. Besides to foot (F), other body regions can be considered as current input and output ports, having their values estimated for the impedance calculation comparatively [10]. For example, the impedance between the neck and the left hand is 60% less than between the left hand and the left foot, resulting in the passage of a greater amount of current (Ohm’s law). By IOM there is the usage of multiple materials simultaneously. Thus, it is recommended to adopt the lowest impedance value aiming to prevent harm. It must be kept in mind that such calculations are considered as a reference possibility, and do not include intravascular and intracardiac devices, which reduce the general reactance.

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EEG ground

Power distribution panel #1

EEG

EKG EKG ground

Power distribution panel #2 CCF © 1999

Fig. 4.2  Ground loop currents. When the equipment connected to the patient is powered by circuits derived from circuit breakers on different panels, the grounding between them may not be equipotential and the patient may carry current between them. (From Levin KH, Luders HO (2000). Comprehensive Clinical Neurophysiology, WB Saunders)

Table 4.1  Correction factor for current path

Path of the electric current passing through the human body From the left hand to the left foot, to the right foot or to both feet From both hands to both feet From the left hand to the right hand From the right hand to the left foot, the right foot or both feet From the back to the right hand From the back to the left hand From the chest to the right hand From the chest to the left hand Left hand, right hand or both hands and buttocks

F 1,0 1,0 0,4 0,8 0,3 0,7 1,3 1,5 0,7

Adapted from: IEC-479-1, Effects of Current on human beings and livestock. Accessed on July 20th, 2021. https:// www.abntcatalogo.com.br/norma.aspx?ID=410528

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Safety Paradigms In a systematic review (including 26,750 publications), Dechent et al. (2002) found four reports of mild adverse effects (burns and skin lesions) associated with TES. As safe as a modern IOM system might be, every precaution must be taken to prevent unwanted events. Perhaps the worst of all causes is to ignore or minimize the risks of accidents, thus providing the cascade of errors and their dire consequences. Indeed, all body tissues and organs can be affected by the current flow.

Electric Stimulation The threats of injury by shock or stimulation are due to the intensity and displacement of the electric current, and the energy. The consequences of the shock are also proportional to the physical variables that act in the propagation of the current through the body, like the frequency of the event, to the body region involved, and to the path through the body. It is considered more relevant if (a) proximal to the heart, (b) involves a large area of the body, and (c) if there is a system integrity disruption (dependent on component impedance and skin characteristic), (d) duration of the flow, and (e) humidity of the environment [4]. These factors affect the intensity of current and energy generated. The intensity of the current will depend on the potential difference, amounts of displaced charges, duration and number of pulses, area of the electrodes, resistance/ impedance of the system, and discharge duration. Other factors should be added, such as the propagation path, the reactance of the body and materials, and the dispersion of energy. The same current intensity over a tissue or body area differs according to its characteristics. For instance, differences in the integrity and physiological conditions of the skin (temperature and skin type) contribute to fluctuating impedance values [12]. The intensity of the stimulus needed to generate a neural action potential and consequent muscle response varies with the duration of the pulse, rheobase, and chronaxie. Using a rectangular pulse, rheobase is related to the smallest value of current applied when considering an infinite pulse width (250 to 1000 μs), while chronaxie is the smallest pulse width to generate muscle contraction, considering twice the rheobase [13]. Parameters that limit the strength of the stimulus make IOM safer. Accordingly, current, charge, and energy are interrelated and if in imbalance, are potentially harmful. Reducing the duration of the stimulus leads to increase in the current threshold and, if too high, it favors electrochemical damage. Increasing the duration of the pulse, on the other hand, can increase the offered charge and consequently the risk of excitotoxic damage.

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Leakage Current or Equipment Malfunction The main concern about current leakage or excessive load output is their potential of finding a pathway through the heart, causing severe arrhythmias like ventricular fibrillation. The presence of central venous access of lower resistance can facilitate this situation. The risk is higher by alternating current and is directly related to its final strength and frequency. The connection of several devices in the OR increases voltage sources and the possibility of grounding paths between the equipment and the patient. However, some simple precautions can minimize these risks [13]: A. Periodic electrical safety testing – identifies possible leakage currents outside the safety limits and possible malfunction of cables and equipment connections that can generate a difference between the current set on the screen and the current offered to the patient. B. Pay attention to the device’s notifications during IOM – modern equipment has its own protection systems that inform the neurophysiologist when there is an inadequate connection. It automatically interrupts stimulation when there is an overload and limits the intensity of stimulation according to the other parameters used (duration, frequency, inter-stimulus interval). For safety reasons, the modern IOM system performs auto-checking when turned on. C. Avoid extension cables, and tin soldered plugs and cables. Preferably, choose touch proof connectors  – these measures help maintain the protective grounding. D. Use stimulus parameters established in the literature. E. Never place the IOM boxes under intravenous drip holders, bladder tubes, or where fluids may enter. Direct contact of liquid with the boxes can reduce impedance to a value lower than that of the plate, turning into an alternative and unwanted area for current flow. Listed situations would be a) incidental leakage of serum, or urine, b) excessive sweating due to thermal blanket. Additionally, avoid locating the grounding plate arranged in a region with a high concentration of hair, which could lead in low contact and greater impedance than desired. The dynamic nature of the skin must be controlled and anticipated, particularly in prolonged surgical procedures, to prevent accidents. Excitotoxicity and Electrochemical Damage Load, charge density, and current intensity can create a peri-cellular electric field due to the movement of ions. During direct stimulation on the nervous tissue, as occurs in subcortical cathodal stimulation, the higher intracellular concentration of negative charges can result in a reduction in proteins. Conversely, anodic cortical stimulation generates a higher concentration of positive ions, facilitating oxidation. Although both processes are correlated to a plethora of neurodegenerative diseases [14, 15], experimental evidence of injury was found only in the animal model after prolonged monophasic stimulation [16]. Yuen et al. in 1981 identified that biphasic

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pulse trains at 50 Hz caused neuronal damage within 15 h of the experiment [17]. It is far more prolonged than that performed in surgical procedures. Specifically, during TES there is an important dissipation of charge in the ratio of 20:1 through the skin and skull [8]. Thus, due to the absence of reports of excitotoxicity in humans, the technique is apparently quite safe, since the intracranial charge and charge density are probably below the lesion threshold. Nevertheless, some cautions deserve attention. Very small electrodes increase the charge density, and the use of 1cm2 electrodes is indicated in DCS [13]. Pulses of 0.2  ms limit the charge when compared to longer pulses and are also preferable. Always use stimuli with parameters well established in the literature and only with the intensity necessary to obtain the responses. Thermal Injury and Burns Considering the energy measured in joules by the relationships between voltage, electric current, and resistance, stimuli from constant electric current vary the intensity of the voltage (Ohm’s law). In extreme cases of intense resistance, the current would be limited by the capacity to increase the voltage inherent in the device, whose intrinsic limit could even prevent its generation. On the other hand, stimuli produced by constant voltage, in the face of changing resistance, tend to produce variable electric current. Thus, energy is also estimated to be unstable. The energy released by the electric current is translated into heat. The best perception of the action of energy on tissues comes from devices used in electrosurgery or diathermy, and their consequent denaturing effect on cellular proteins and tissues: coagulation and vaporization. During fever of 40 degrees, some enzymes can have their tertiary and quaternary conformation reversibly modified, partially altering their function. Above 50 degrees, denaturation for more than 6 minutes leads to cell death. Thermal injuries occur due to inadequate heat dissipation, and their incidence in IOM is estimated at 0.01%. As previously described, energy is related to current intensity, pulse duration, and resistance, and its empirical safety limit in TES is 50 mJ at 1 k resistance [6, 18]. Very short pulses increase energy and can facilitate thermal injury. Durations of 0.01 ms should be avoided in DCS. Ideally, the pulse duration should be adjusted to tissue chronaxie, but this parameter is not always known or the adjustment feasible. Evidence suggests that the average chronaxie in DCS MEP is 0.2 ms [19], which is why stimuli of this duration are preferable and considered safer. Another way to minimize the risk of thermal injury is to avoid intensities above what is needed for optimal responses and to avoid high intensities in TES using a pulse duration of 0.05 ms. The effects of the controlled current expended during the somatosensory evoked potential (SSEP) or TES are easy to quantify [17], even though the heat generated can affect structures unevenly. The calculated current densities in direct cortical MEP application range between 0.029  mA/cm2 and 0.057 mA/cm2, thus far below the safety limit of 14.29 mA/cm2 [4].

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Electrocautery represents a direct transmission of heat to the tissue, with no current flowing through it, since the pathways are contained at a single end. It employs high frequencies that do not depolarize nerves and muscles but interfere with neurophysiological screen recordings. Yet, the current transits between the tip and the plate positioned in contact with the patient’s skin. Generally, the plate has a large surface area, which reduces the local charge density and generates less heat. But if the plate comes loose, or in presence of malfunctions or breaks in the cable, current can leak through lower impedance points and nearby electrodes. In these cases, IOM’s needle electrodes are potentially harmful because their small surface area causes high energy density and heat, with possible burns. Whenever possible, IOM equipment, cables, and connections should be kept away, and needle electrodes should not be placed close to the plate. Preventive Measures There is the risk posed by a device without adequate preventive maintenance to cause the passage of electrical current beyond what is recommended. It could cause tissue damage near the entrance, or at a distance depending on the intensity. Yearly system check-up hinders the risk of accidents. Reuse of electrodes poses a higher risk of injury since in this case the electrodes have a far higher resistivity up to a factor of 10,000 [4]. It is strictly not recommended.

Adverse Effects Biting and Movement In TES, some degree of movement is always expected, and the proximity of the stimulus point to the temporal muscles and trigeminal nerve promotes strong activation of the masseter muscle and risk of tongue biting. The incidence of such an event is approximately 0.2%, and the use of soft protectors between the teeth (silicone protectors or gauze roll) is indicated whenever the technique is used [17, 20]. Rigid guards should be avoided as they offer the additional risk of tooth breakage. Injuries are usually restricted to bruising or minor lacerations of lips and/or tongue, and the need for surgical repair is rare (Fig. 4.3). Body movement in TES can be reduced by using more selective montages such as C3-CZ, C4-CZ, C1-C2, and midline instead of C3-C4 and avoiding the use of high stimulus intensities (more details of topographic-guided MEP refer to Chap. 9). Not least, good communication between neurophysiologist and surgeon is essential so that the stimulations are performed at a timely moment within the times of the surgery. Thus, the surgeon can quickly stop manipulation near a neural structure so that TES can be performed.

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Fig. 4.3  Bite injury due to TES

Fig. 4.4  Seizure triggered by DCS

Seizures and Afterdischarges Particularly, patients with a history of epilepsy, diffuse brain lesions, and during the use of the Penfield technique are more likely to have ictic or epileptiform discharge events after direct electric stimulation [5, 17, 18]. Seizures and afterdischarges are rare with high-frequency TES (0.03%) [18], but may occur in DCS or direct subcortical stimulation, especially when the 50-60 Hz technique is used. During direct brain stimulation, there is an estimated incidence of seizures in 5 to 20% of patients using low frequency, while with high-frequency technique the incidence is about 1% [18] (Fig. 4.4). The use of cold serum irrigation is recommended to control the event (the use of anticonvulsant drugs may prevent language mapping, although its use in refractory cases is strongly advised). For more a comprehensive understanding read Chap. 17.

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Arrhythmias Cardiac arrhythmias are rarely reported in the literature. Besides the excessive current output and its intracardiac passage, arrhythmias can occur by electric stimulation at brainstem autonomic centers, especially during the mapping of lesions in IV-ventricle floor [18]. The lack of reports might be related to low morbidity rate.

Risk Due to the Use of Invasive Electrodes Bleeding and Bruising The placement of cortical grids or D-wave electrodes in the epidural/subdural space can potentially cause traction and rupture of vessels leading to bleeding or hematoma formation. However, usually, the surgeon performs the maneuver quite delicately and no morbidity has been reported so far [13]. Infections To record responses, needle electrodes are inserted sub-dermally or into muscles bellies which pose a risk of local infection. Prevention includes skin preparation by cleaning it with 70% alcohol or alcoholic chlorhexidine. Areas where the skin is not healthy or where there are signs of infection should be avoided. In addition, the neurophysiologist should also protect himself/herself from contact with patient fluids and from sharp injuries by using personal protective equipment such as gloves and goggles. Needle electrodes, cortical grids, D-wave electrodes, and stimulators should be sterile and discarded after use.

Contraindications to IOM The risk-benefit of IOM must be considered and weighted in face of relative contraindications, like pacemakers and/or implantable bioelectric devices, DBS, epilepsy, vascular clips or shunts, and skull deformities. Adaptations of the technique can enable testing targeted to patients’ needs.

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Electronic Implants Modern electronic devices are built with amplification of electrical and motion signals to detect and trigger responses or set for continuous or alternate stimulation. It allows for increased sensitivity to those who are interested in correcting dysfunction but leaves them more subject to interference, either electrical or mechanical, originating from the organism itself or external, as well as exogenous magnetic and radioactive. The list includes pacemakers of fixed or variable demand (cardiac or vagus nerve), deep stimulators of the nervous or substance release system, cochlear implants, etc. In general, they have filters that select the frequency of deflagration, or mechanisms that prevent the passage of currents, setting the activation of safety modes. However, the possibility of interference is common to all, with greater or lesser risk of deregulation of the device [21, 22]. Yellin et al. (2015) described the successful use of TES in two pediatric patients with cochlear implants [23]. Thus, risks and benefits should be analyzed according to patient’s needs. Pacemakers Specially about pacemakers, their circuits amplify, filter, and identify the cardiac potentials, correcting bradycardia and tachycardia. External electrical interferences can provoke dysfunction, leading to inhibition, asynchronous reversion, or inappropriate defibrillation [24]. A strong electrical charge could damage its components or overheat the electrode-myocardia junction without possible repair. So electrical bistoury, thermocautery, MRI, radiotherapy, radiofrequency, diathermia, and TES are normally avoided. Several protection mechanisms have been created to avoid continuous current to enter the pacemaker or to short cut high-intensity currents before they damage it. Such mechanisms are bipolar electrodes, electronic filtering, and spectral detection. Under a skilled specialist, the pacemaker program can be modified during a specific procedure to stand a hostile situation. The recommendation is that during the IOM to rely on the presence of a technician in the OR for adjusting the specific configuration and tracking of the device. If necessary, set to asynchronous mode [22] (Fig. 4.5). A practical alternative is also to modify the stimulation frequency to produce desynchronization between the electronic device artifact and the wave to be studied, or the application of cardiac stimulus with bipolar electrodes, reducing the extension of the artifact.

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a

b

Fig. 4.5  MAS, female, 75y.o., going through a L3-L5 lumbar stenosis decompression. TES was performed with C3-C4 stimulation, train of 6 pulses, 0,5 ms duration, 4 ms interpulse interval, 300 V. The patient had a bicameral pacemaker due to total AV blockage. Immediate after the positioning of the patient, the cardiologist turned the pacemaker to an assincronic function, which stimulated the ventricle with 6,5  V, 1  ms duration, and 80  bpm. In an assincronic function the pacemaker was not influenced for an external electrical source and TES was registered several times during the decompression maneuver. (a) Pacemaker registration during TES. (b) TES

Troubleshooting Electrical Artifacts Artifacts or noise are broadly defined as any signal captured that is not of interest to the purpose of the study. Usually, biological signals of interest are made up of a set of frequencies. Thus, in the examination of SSEP, muscle contractions studied on EMG, electrocardiogram, or respiratory movement captured during the EEG, environmental noise during language testing would be characterized as noise. On the

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other hand, eye movement recorded during sleep is a useful activity for staging the REM phase, or even drowsiness, aiding in the diagnostic interpretation. Noises/ artifacts are, therefore, signals from multiple sources (biological and non-­biological) registered within the chosen spectrum of the frequencies to be analyzed, or which impair their interpretation. The first action to minimize the effects of the artifacts is knowing the frequency range of the biological signals under study and applying a bandwidth filtering to improve their recording but not causing distortion to the point of misinterpretation [25]. Additionally, limiting the time window with an appropriate sweep time for detecting the studied potentials mitigate irrelevant signals. Some simple measures can help, like (a) keeping the IOM system (including recording boxes) distant from the potential sources of electromagnetic fields (electrocautery, microscopes, radioscopy), (b) not sharing electrical sockets, (c) joining or braiding the electrodes cables. There is no single protocol to be followed to minimize or eliminate noise, although recognizing the most common ones surely helps in dealing with its source. A helpful sequence could be (a) correctly distinguish between an artifact and an electrode leakage, break or disconnection, (b) guide following actions according to the most likely suspicions. Unfortunately, it is not uncommon to be unable to identify where the major cause is coming from in environments with numerous competitors.

Troubleshooting in Non-biological Electrical Artefacts (a) Check if the sockets are grounded and preferably on a mutual ground, i.e., exclusively for the flow of charges from medical equipment used to care of that patient (do not connect the patient directly to this electrical ground). Connecting to outlets with different grounds can generate uneven ground loops. (b) All equipment connected to the patient must have its own isolation system, producing no leakage currents greater than 10–20 μA (optimal). It is assumed that the insulation tests and prophylactic maintenance of the equipment are carried out routinely to ensure good and proper electrical operation, with leakage currents through the chassis up to 100  μA.  The devices must be previously ­connected to their connection with the patient, and turned off only after proceeding with their disconnection, ensuring that leakage currents do not move. (c) 50 Hz or 60 Hz artifacts can come from the socket itself, whose grounding is not adequate, network overload due to the amount of equipment connected, proximity between devices (Video 4.1) and/or crossing of capture and stimulation wires and cables, power cables, etc. (Video 4.2). Stimulation outside harmonic frequencies helps to reduce this type of artifact (Video 4.3). Expandable equipment for patient care should be turned off and disconnected from the network.

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a

b

c

Fig. 4.6 (a) Loss of motor potentials in left tibialis anterior muscle. (b) Impedance test showing same impedance value. (c) Checking of electrodes revealed bending and electrode breakage

(d) The electrodes and stimulators must be in proper conditions of use, and have their impedances correctly assessed. Higher than expected impedances can indicate wire breakage, increased resistivity, or adhesion, and zero impedances can indicate the formation of electrical bridges (Fig. 4.6). Additionally, unbalanced impedance values between a pair of electrodes (>1kOhms) should be promptly corrected. (e) The use of high- and/or low-frequency filters should be done with discretion, considering the changes they generate on biological signals. Over-filtration may lead to the error of generating waves that do not correspond to physiological signals.

Troubleshooting in Biological Electrical Artifacts (a) Use of differentiated parameters (scan time, stimulation frequency, mediation, disposition of capture electrodes) can minimize the recording of artifacts. (b) Environmental and patient control: (a) temperature stability prevents prolongation of latency due to temperature drop and alteration of signal amplitude; (b) control of level of consciousness during anesthesia using EEG and spectral edge frequencies avoid administration of drugs bolus or that modify the generation or capture of signals (Video 4.4).

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Conclusion Understanding basic concepts of bioelectricity and its effects on the human body greatly improves the recognition of possible risks to which a patient is exposed during IOM. When strictly performed within the recommended parameters, IOM does not cause irreversible cellular damage and is not related to high morbidity. Mostly, events are related to patient movements (which may disturb the surgeon), seizures, and bite injuries. However, under inappropriate conditions, like excessive electrical current output or passage of current through the heart, the risk of excitotoxicity, electrochemical and thermal injury, or arrhythmias increases. The rich electromagnetic environment in OR can generate artifacts or noise that impair the interpretation of the recorded responses. It is part of a good practice of the neurophysiologist to understand these situations to correctly deal with them.

References 1. Halliday D, Resnick R, Walker J. Fundamentals of physics. 10th ed. Wiley Publisher; 2013. 2. Chaves A. Basic physics: electromagnetism. 1st ed. LTC Publisher; 2007. 3. Bauer W, Westfall GD, Dias H. Physics for university students: electricity and magnetism. 1st ed. AMGH Publisher; 2013. 4. Dechent D, Emonds T, Stunder D, Schmiedchen K, Kraus T, Driessen S. Direct current electrical injuries: a systematic review of case reports and case series. Burns. 2020;46(2):267–78. https://doi.org/10.1016/j.burns.2018.11.020. 5. Dineen J, Maus DC, Muzyka I, See RB, Cahill DP, Carter BS, Curry WT, Jones PS, Nahed BV, Peterfreund RA, Simon MV. Factors that modify the risk of intraoperative seizures triggered by electrical stimulation during supratentorial functional mapping. Clin Neurophysiol. 2019;130:1058–65. 6. IEC-479-1. Effects of current on human beings and livestock  - part 1: general aspects. Publication 479–1 International Electrotechnical Commission; 1994. 7. Brazilian Standard of ABNT NBR IEC (2012) 60601–1 addendum 1, subsection 3, page 36 and subsection 4.8; 2016. 8. Brazilian Standard of ABNT NBR IEC 60601-1. 2nd edition. 2010:p.180. https://www.abntcatalogo.com.br/norma.aspx?ID=410528. Accessed on 20 July 2021. 9. Misulis KE.  Basic electronics for clinical neurophysiology. J Clin Neurophysiol. 1989;6(1):41–74. 10. Kindermann G. Electric Shock. 4th edition of the author. Santa Catarina: LabPlan; 2013. 11. Burgess RC. Electrical safety. In: Levin KH, Chauvel P, editors. Handbook of clinical neurology, vol. 160. Elsevier; 2019. p. 67–81. 12. Brazilian Technical Standards Association (ABNT) NBR 5410. Low voltage electrical installations. 2004 (revised version 2008). pp. 30–31. 13. Macdonald DB, Seidel K, Shils JL. Safety. In: Deletis V, Shils JL, Sala F, Seidel K, editors. Neurophysiology in neurosurgery – a modern approach. Elsevier; 2020. p. 581–96. 14. Gandhi S, Abramov AY.  Mechanism of oxidative stress in neurodegeneration (review). OxiMed and Cellular Longevity. 2012:1–11.

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15. Matthew D, Matthew R, Namakkal SR, Victor DU, Jianhua Z.  KEAP1  – NRF2 Signalling and autophagy in protection against oxidative and reductive proteotoxicity. Biochem J. 2015;469(3):347–55. 16. Merril DR, Bikson M, Jeffreys JGR. Electrical stimulation of excitable tissue: design of efficacious and safe protocols. J Neurosci Methods. 2005;141:171–98. 17. Macdonald DB.  Safety of intraoperative transcranial electrical stimulation motor evoked potential monitoring. J Clin Neurophysiol. 2002;19(5):416–29. 18. Macdonald DB, Skinner S, Shills J, Yingling C. Intraoperative motor evoked potential monitoring – a position statement by the American Society of Neuropysiological Monitoring. Clin Neurophysiol. 2013;124:2291–316. 19. Abalkhail TM, Macdonald DB, AlThubaiti I, AlOtaibi FA, Stigsby B, Mokeem AA, AlHamoud IA, Hassounah MI, Baz SM, AlSemari A, AlDhalaan HM, Khan S. Intraoperative direct cortical stimulation motor evoked potentials: stimulus parameter recommendations based on rheobase and chronaxie. Clin Neurophysiol. 2017;128(11):2300–8. https://doi.org/10.1016/j. clinph.2017.09.005. Epub 2017 Sep 28 20. MacDonald DB, Deletis V. Safety issues during surgical monitoring. In: Nuwer MR, editor. Intraoperative monitoring of neural function, Handbook of clinical neurophysiology, vol. 8. Amsterdam: Elsevier; 2008. p. 88298. 21. Merrit WT, Brinker JA, Beattie C. Pacemaker-mediated tachycardia induced by intraoperative somatosensory evoked potential stimuli. Anesthesiology. 1988;69:766–8. 22. Schneider R, Machens Q, Bucher M, Raspé C, Heinroth K, Dralle H.  Continuous intraoperative monitoring of vagus and recurrent laryngeal nerve function in patients with advanced atrioventricular block (rapid communications). Langenbeck's Arch Surg. 2016;401(4):551–6. https://doi.org/10.1007/s00423-­016-­1433-­0. Epub 2016 Apr 30 23. Yellin JL, Wiggins CR, Franco AJ, Sankar WN. Safe transcranial electric stimulation motor evoked potential monitoring during spinal fusion in two patients with cochlear implants. J Clin Monit Comput. 2016;30:503–6. 24. Elmqvist R, Senning Ä. Implantable pacemaker for the heart. Proceedings of the second international conference on medical electronics, Paris. Jun 24–27, 1959. 25. Burgess RC. Filtering of neurophysiologic signals. In: Levin KH, Chauvel P, editors. Handbook of clinical neurology, vol. 160. Elsevier; 2019. p. 51–65.

Chapter 5

Central Nervous System Anesthesia: Asleep Approach Nelson Mizumoto

Abbreviations BBB blood-brain barrier BIS Bispectral Index CBF cerebral blood flow CBV cerebral blood volume CMRO2 cerebral metabolic rates CNS central nervous system CPP cerebral perfusion pressure ECoG electrocorticographic EEG electroencephalography Hb hemoglobin ICP intracranial pressure IOM neurophysiological monitoring MAP median arterial pressure MEP motor-evoked potential SSEP somatosensory evoked potential TIVA total intravenous anesthesia

N. Mizumoto (*) Anesthesiology Coordinator at the Neurosurgery Department, Clinical Hospital of University of Sao Paulo Medical School, Sao Paulo, Brazil © The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 S. M. Verst et al. (eds.), Intraoperative Monitoring, https://doi.org/10.1007/978-3-030-95730-8_5

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Intracranial Pressure (ICP) and Cerebral Blood Flow (CBF) ICP normal range values are 10–15 mmHg and result from the interaction of liquor volume with the intracranial pressure, the cellular interstitial fluid, and the water volume inside neurons and astrocytes. Excessive water in the brain results in cerebral edema thus affecting its plasticity. Brain swelling leads to loss of vascular reactivity and causes increase in the cerebral blood volume. The intracranial compensation mechanism relieves the ICP increase when small volumes are added inside the skull [1, 2] When the volume of one of the ICP constituents increases, this compensation mechanism decreases the volume of the other players in order to keep a constant ICP and to prevent the reduction of the CPP.

Cerebral Blood Volume and Cerebral Blood Flow The intracranial blood volume may increase due to the augment of arterial dilation caused by increased cerebral metabolism, hypercapnia, hypoxia, or by the action of encephalic vasodilator drugs. The loss of arterial constriction (e.g., loss of cerebral autoregulation) elevates cerebral blood volume, which may worsen in the presence of systemic hypertension. Moreover, increased intracranial venous blood can occur with the obstruction of the brain’s venous drainage system, either by expansive intracranial processes or by increased extracranial venous resistance such as high intrathoracic pressure, or yet, due to excessive neck rotation or patient’s head positioned below the heart. Factors which alter cerebral blood flow  According to Ohm’s law, the flux of fluids inside a rigid tube depends: (a) on the difference between the entrance pressure and the exit pressure in this tube, (b) as well as the fluid resistance in the tube. The flux equation is obtained by considering the fluid resistance degree as the tube’s radius increase, and the fluid resistance increase as long is the tube; or more viscous is the fluid (Hagen-Poiseuille relation):

F=

( P1 − P 2 ) . r 4 8.l.η



[wherein F is the flux, P1 the entrance pressure, P2 the exit pressure, r is the tube radius, I the tube’s length, and η is the fluid viscosity]. That equation is applied to the Newtonian fluids which yield flux without turbulence inside rigid tubes. As a rational exercise, we may apply the equation to the blood flux in the cerebral artery and the arterioles, despite the arterial variation in diameter. Therefore, we consider F as the encephalic blood flux, P1 as the median arterial pressure (MAP), P2 as the intracranial pressure (ICP), r as the encephalic

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artery radius, I as the length of encephalic circulation, and η as the blood viscosity. This equation does not apply to brain capillaries due to the size of the red cells in relation to the capillary lumen. The mean global blood flow to the brain is approximately 53.5 ml/100 g/min. Cerebral blood flow and cerebral blood volume may vary during anesthesia, as the diameter of cerebral arteries and arterioles changes with cerebral metabolic activity, arterial carbon dioxide (PaCO2), and/or arterial oxygen (PaO2) concentrations as well as the systemic arterial pressure.

 erebral Blood Flow (CBF) and Cerebral Metabolic C Rate (CRMO2) Under normal conditions the brain controls its blood flux to maintain the supply of energy substrate according to its needs [3–5]. In other words, the brain coordinates the cerebral metabolic requirements and the brain vascular reactivity by keeping constant the relationship between cerebral blood flow (CBF) and cerebral oxygen metabolic rate (CMRO2). Therefore, when the metabolic rate is reduced, the cerebral blood flow is reduced as well, as it occurs during barbituric-induced coma. Conversely, in the convulsive crises the metabolic rate and the blood flux are both increased [6]. Conversely, anesthetics which relax the smooth muscle fibers of cerebral arteries disrupt that relationship and despite the metabolic rate reduction, the halogenates increase cerebral blood flow due to the arterial dilation. Barbiturates which induce vasoconstriction keep constant the relationship between decreased cerebral metabolic rate and reduced cerebral blood flow. Therefore, in the normal brain, the relationship between cerebral blood flow and cerebral metabolic rate is constant (CBF/CMRO2 = 15), with the blood flow being modified by the metabolic activity. The factors that modify that relationship are (a) halogenate anesthetics (despite reducing metabolic rates they increase blood flow, thus changing the relation CBF/CMRO2); and (b) the relationship between metabolic rate and blood flow is modified in the brain as a result of traumatic injury and in the swollen peritumoral areas as vascular reactivity is compromised.

Cerebral Blood Flow and PaCO2 Carbon gas concentrations in the blood modify both the diameter and flow in the arteries and arterioles [7, 8]. Hyperventilation causes hypocapnia, also known as hypocarbia, which leads to liquor alkalinization, cerebral vasoconstriction, and reduced CBF. Respiratory acidosis or alkalosis change CBF whereas blood metabolic acidosis or alkalosis have almost no effect on the CBF because there is no immediate passage of bicarbonate or hydrogen ions through the (healthy/intact)?

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blood-brain barrier (BBB). CBF is altered in 2–3% with 1  mmHg change in PaCO2 [8]. The normal global CBF is 52 ml/100 g/min. When PaCO2 is at 20 mmHg the intense vasoconstriction excessively reduces the blood flow (20 to 25 ml/100 g/min) and may cause cerebral ischemia by reducing neuron activity and flattening the electroencephalographic (EEG) tracing. Cerebral vasodilator drugs such as halogenate barbiturates displace the CO2 curve to the left. Cerebral vasoconstrictor drugs (e.g., barbiturates, benzodiazepines, and etomidate) shift the curve to the right. The vascular reactivity to CO2 is ineffective in the arteries present in the peritumoral area. In that area the blood flow is augmented, providing an increased supply of oxygen which is known as luxury perfusion because such excess of blood and extra oxygen supply is not needed by the peritumoral nervous tissue [9] .

Cerebral Blood Flow and Arterial Pressure CPP is the gradient difference between median arterial pressure (MAP) and ICP, CPP = MAP-ICP. The brain has autoregulation mechanisms which keep constant the blood flow when the arterial variation occurs within certain limits. Therefore, cerebral arterial dilation occurs during a systemic arterial hypotension whereas cerebral arterial constriction occurs during a systemic arterial hypertension. CBF may be understood as fluid flow in conduction vessels. In other words, because of the existing variation in the encephalic perfusion pressure, the radius of arteries and arterioles change to keep CBF constant. Such autoregulation is effective with arterial median pressures within the lowest limit of 50 mmHg and the upper threshold of 150 mmHg [10, 11]. When the MAP is higher than 150 mmHg, the contraction of the muscle fibers in arterioles becomes ineffective, which increases brain blood flow and volume. Situations that modify vascular reactivity to MAP variation are as follows: (a) the self-regulation curve threshold where the flow is constant is shifted to higher values with hypercapnia or to lower values with hypocapnia; (b) drugs that cause brain vasodilation, such as halogenated anesthetics, shift the autoregulation from the upper limit to lower blood pressure values; and (c) CBF self-regulation capacity is reduced in damaged areas of the brain, such as those presenting peritumoral edema.

 ffects of Anesthetics on the Cerebral Blood Flow E and the Metabolic Rate Inhaled halogenated anesthetics of major or lesser intensity (halothane, isoflurane, sevoflurane, and desflurane) reduce brain metabolism [12, 13], depending on the administered dose concentration. Nevertheless, they act on the smooth muscle fibers

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of encephalic arteries and arterioles inducing vasodilation and increased blood flow. The higher the dose concentration of halogenated anesthetic, the greater the shift from the autoregulation upper limit curve (150  mmHg) to lower values. Besides considering the effect of halogenated anesthetics on CBV, the effect on systemic peripheral resistance should also be considered, as it may cause a certain degree of systemic arterial hypotension. Sevoflurane shows a lesser impact on the encephalic vascular reactivity and causes a minor effect on encephalic vasodilation than the other halogenated anesthetics [14]. Enflurane, when associated with deep hypocapnia, can generate EEG readings alike the state of epilepsy [15]. Nitrous oxide is associated with increased CBF and the cerebral metabolic rate [16, 17], but these effects can be minimized with intravenous anesthetics that reduce metabolic rates and cause vasoconstriction. Except for ketamine, intravenous anesthetics cause cerebral vasoconstriction which increases brain activity [18, 19]. The vasoconstriction reduces cerebral blood volume and intracranial pressure. As the reduction in blood flow is due to a depressant action on the neuron’s metabolic rate, at adequate levels it does not cause brain damage since it also reduces the oxygen demand. Although anesthetics reduce the metabolic rate, they do not fully protect nerve cells from the induced blood flow reduction resulting from deep hypocapnia. Intravenous barbiturates decrease the functional activity of neurons. In other words, they reduce the neurotransmission-induced activity [20, 21] in those brain areas that still respond to vascular reactivity mechanisms [22] . Barbiturate-induced coma aiming at metabolic reduction should be monitored through continuous EEG activity, as it has not an additional effect in reducing the intrinsic activity of neurons and the excess of barbiturates causes significant depression on the cardiovascular system plus arterial hypotension. Methohexital may cause EEG activity and induce seizures in epileptic patients [23]. It was used in the past to evoke epileptic activity for mapping brain activity in patients who had no brain activity due to depression caused by deep general anesthesia during craniotomy. Like barbiturates, etomidate reduces the metabolic rate and CBF [24, 25], but not in a linear fashion. The maximum reduction of CBF occurs with a smaller dose than that necessary to reduce the maximum possible metabolic rate, which suggests that etomidate acts in two distinct pathways: direct action on cerebrovascular constriction and on suppression of metabolic activity [26]. As previously mentioned, etomidate can trigger tonic-clonic muscle activity and EEG spams like seizures [27, 28], which enabled its use for brain stimulation in patients undergoing general anesthesia with EEG activity suppression, in replacement of methohexital. However, dose increases of etomidate cause depression of brain activity [29] . Hypothermia reduces neuron intrinsic activity because it decreases the total metabolic activity by 7% per each reduced degree of temperature in the brain [30, 31]. Benzodiazepines reduce in approximately 25% the metabolic rate and CBF. The flow reduction seems to be related to the metabolism [32, 33]. and to the reduction in intracranial pressure. Flumazenil reverses the effects of benzodiazepines on CBF,

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CMRO2, and ICP, so it may have unintended effects when used to reverse anesthesia [32]. Propofol reduces the metabolic rate, cerebral blood flow, and intracranial pressure [34–36]. However, since it also reduces the systemic blood pressure [37], a red flag should be raised to the risk of reducing cerebral perfusion if systemic arterial hypotension occurs [38, 39] in neurosurgical patients. Opioid anesthetics have the least direct effect on cerebral blood flow, metabolic rate, and intracranial pressure [40]. Ketamine is a potent cerebral vasodilator capable of significantly increasing CBF [41] which may worsen the patient’s condition with pre-existent intracranial hypertension or seizures [42]. Succinylcholine may increase ICP, likely due to ICP increases caused by the nociceptive stimuli reaching the brain [43–45]. Therefore, before the administration of succinylcholine, deep anesthesia must be instituted with anesthetics that reduce ICP in patients with intracranial hypertension. Competitive muscle relaxants should not be used when monitoring with motor evoked potential (MEP). If the use of competitive muscle relaxants is necessary, they must have their action reversed before starting motor stimulation [46].

General Anesthesia and the CNS Monitoring When deep enough anesthesia is administered to reduce the CNS metabolic rate, a relaxed brain with a reduced volume occurs that does come out of the cranial space. This facilitates the surgical handling by the neurosurgeon because the deeper the anesthesia the lower the metabolic rate and smaller the brain volume. Such brain-­ volume reduction is due to cerebral arterial vasoconstriction, which depends on the arterial regulation, induced by the changes in neuronal metabolic rates. However, too deep anesthesia may cause unintended adverse effects on the neurosurgical procedure when intraoperative monitoring of the CNS is performed. Anesthetic drugs may depress evoked sensitive and motor responses in a major or minor intensity, depending on the chosen anesthetic and the administered concentrations. Therefore, it is crucial the understanding of CNS physiology and of its interactions with the effects of systemic changes and/or the effects of the administered drugs. The goal of intraoperative monitoring is the prompt detection of ischemic aggression in the brain or in the spinal medulla, to stop or decrease the intensity of surgical handling, thus avoiding harmful and irreversible events. Moreover, one should keep in mind other factors that hinder the CNS monitoring such as: (a) hyperventilation that induces hypocapnia, followed by vasoconstriction and ischemia; (b) hypothermia that decreases neuronal metabolism; (c) arterial hypotension that causes ischemia; and (d) mechanical compression of peripheral nerves which affects the conduction of nerve stimuli. Intravenous and inhaled anesthetics affect the neural synaptic and axonal functional activities, and the response depends on the affected pathway and on the

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mechanism of action of the anesthetic agent. In other words, the inhibition effect may be direct or indirect, depending on changes between inhibitory or excitatory inputs [47]. The synaptic effects of inhalation anesthetic agents are more highly dependent responses on the synaptic function that will have marked reductions in amplitude and increases in latency. The use of intravenous anesthetics will require much higher doses to achieve the same effect. Intravenous anesthetics like etomidate, ketamine, and fentanyl allow better registry of the evoked motor potential than halothane. For intraoperative CNS monitoring and brain mapping, general anesthesia cannot be too deep otherwise the interpretation of the electrocorticographic (ECoG) readings will be difficult. Conversely, two shallow anesthesia may induce awakening, so it is important to previously orient the patient for the possibility of awakening during ECoG.  Sudden and agitated awakening may lead to excitation, heart frequency, and arterial pressure increase, causing elevation of cerebral blood volume and augmentation of brain volume. In cases of too much excitation, convulsive crises may occur with the disorderly activity of brain neurons, brain-volume increase, and risk of cortical hemorrhage. In such extreme situation the cerebral cortex must be perfused with a very cold physiologic solution to reduce neuronal metabolism and to stop the convulsive crisis. If such procedure is not enough to cease the epileptic activity, anticonvulsant anesthetic drugs such as propofol (10–30 mg) in bolus should be administered. If still necessary, midazolam (1–2 mg) in bolus can be administered as well. In the latter case, consider that the subsequent recording of ECoG activity may be impaired if high doses of benzodiazepines were administered [48]. The use of a muscle relaxant impedes the MEP registry and when its administration is necessary, the use of an antagonist should be administered before the next motor-evoked potential reading [46]. Under some circumstances, too deep anesthesia affects the interpretation of the EcoG reading, even after superficializing the anesthetic dose. If cortical mapping is not possible, anesthetic drugs that increase activity in brain foci should be administered. Methohexital was the most used anesthetic to evoke this excitement [49, 50], but due to the irregular response regarding the required dose and the intensity of the epileptic crises, it was replaced by other drugs. Low-dose etomidate may activate epileptic foci whereas in high doses it may depress the entire brain [27, 51]. Patients who develop intraoperative convulsive crises may be kept under anticonvulsant drugs of long duration, such as phenytoin, during the post-surgery period [48]. The choice of short half-life intravenous hypnotics (propofol, dexmedetomidine) with remifentanil and/or fentanyl has been frequently adopted as it permits rapid anesthesia superficializing and brain volume reduction. When halogenated inhalation anesthetics are used, they should be administered in low concentrations and in association with other intravenous anesthetics. When choosing the anesthetic drug, it should be considered its effects on ECoG and on the evoked sensitive and motor potentials. An exchange of ideas with the neurophysiologist who will perform the monitoring could be very productive.

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 lectroencephalogram (EEG), Bispectral Index (BIS), E and Evoked Potential The anesthetized state is comprised by two factors: (a) sedation/hypnosis (mental blocking); and (b) analgesia (sensitive suppression). Deep hypnosis without analgesia does not prevent hemodynamic changes in response to nociceptive stimuli. Conversely, deep analgesia does not guarantee an unconscious state. Therefore, deep anesthesia is obtained with a combination of anesthetics or by an anesthetic drug which yields both anesthesia and unconsciousness, simultaneously [52]. Those two components are intimately associated since the unconscious state impedes pain perception, which could be magnified if the patient were awake during the procedure whereas the lack or insufficient analgesia could induce patient’s awakening due to the pain caused by the nociceptive stimulus [53]. EEGs to study the action of anesthetic drugs in the CNS have been used for years, and an extensive EEG data bank of patients submitted to diverse types of anesthetics is currently available [54]. In anesthetized patients the EEG readings show a shift from high-frequency and low-amplitude waves – which are present in the awake state – to lower frequencies and higher amplitude waves, characteristic of deep anesthesia. High-frequency low-amplitude occurs predominantly in light anesthetic levels. Alpha-waves (8–12 Hz) appear with the increase of anesthetic depth and replace the higher frequency β-activity (13–30 Hz). As the anesthesia progresses, low-­frequency high-amplitude θ-waves (5–7 Hz) and δ-waves (1–4 Hz) occur [55]. The bispectral analysis (BIS) of the EEG by a mathematical process has obtained a bispectral index which is dependent on the coherence measure of the EEG quantitative components [56]. The BIS obtained by processing of EEG parameters is used to measure the anesthesia depth, thus helping to schedule faster awakening from anesthesia and reduced recovery time, which are associated with keeping the BIS between 50 and 65 [57, 58]. Monitoring with BIS helps in the anesthetic drug titration to obtain the desired depth and reduces the consumption of anesthetics, whether inhaled or intravenous [59], which contributes to the reduction of adverse side effects, such as arterial hypertension or hypotension as well as post-operative cognitive dysfunctions during recovery [60, 61]. During neurosurgery with CNS monitoring, a too deep anesthesia can make it difficult to obtain adequate readings for possible mechanic aggression to certain CNS areas. The use of certain anesthetic agents that further depress the CNS can also make monitoring difficult. Therefore, the combined use of EEG, BIS, and evoked potentials will allow more accuracy in the anesthetic dose adjustment and the adequate level of analgesia and hypnosis for each patient, while avoiding too deep anesthesia which would hinder the CNS monitoring. Total intravenous anesthesia (TIVA) facilitates the evoked monitoring interpretation when compared to balanced anesthesia [46, 62, 63] being preferred by neurophysiologists during intraoperative monitoring.

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Drugs with neurophysiologic and pharmacokinetic properties, such as propofol, remifentanil, ketamine, and midazolam, favor the better intraoperative quality of the MEPs and reduce surgical morbidity [64] because they facilitate the CNS mapping and interpretation. Propofol is the most used anesthetic to perform ECoG recording during surgeries requiring the cerebral cortex mapping, although there are some case reports in the literature correlating propofol with the induction of tonic-clonic seizures, as above mentioned [63]. Dexmedetomidine is a short-acting α-2 agonist with no respiratory-depressive effects and properties of anxiolysis, analgesia, sedation, and sympatholysis. As it does not interfere with the motor-stimulatory effect and ECoG activity, it has a good indication for awake craniotomy in epileptic patients [63]. Further details on awake-­ approach anesthesia are addressed in Chap. 15. Synthetic opioids (alfentanil, fentanyl, sufentanil, and remifentanil) can be used in awake craniotomy as they do not have a significant risk of causing perioperative seizures or changes in ECoG activity. However, high doses of synthetic opioids can increase interictal spike activity [65–68]. Note that myoclonus, which occurs as a side effect of etomidate, coincides with an increase in the components of the somatosensory evoked potential (SSEP), which could indicate a disinhibitory or excitatory cortical effect, although in spike-wave complexes it is seen at the EEG after etomidate [69]. The pharmacokinetics and pharmacodynamics of anesthetic drugs are modified in senior patients and may lead to deep and lasting effects or even unintended side effects. BIS is a useful monitoring tool to help adequate titration of anesthetics in elderly patients [61, 70]. BIS has a good correlation to assess the anesthesia depth regardless of age, even though age-related differences in the EEG may exist in the normal population. However, BIS values can be much lower during anesthesia when there is senile dementia [71], probably due to extensive atrophy of the cerebral cortex. Besides monitoring anesthesia depth with BIS, evoked potentials also help in this assessment. BIS gradually increases during the superficializing of anesthesia, helping to monitor awareness and end of anesthesia. However, the auditory evoked potential better identifies the transition state between awake and sleeping than BIS [72]. Similarly, to BIS, auditory evoked potential helps titrate the anesthetic dose, improving post-anesthetic recovery [73]. Intraoperative neurophysiological monitoring (IOM) using SSEPs and MEPs contributes to the intraoperative decision with the patient under general anesthesia, thus reducing surgical risk. However, the IOM is under the influence of the anesthetic agent administered since both inhaled and intravenous anesthetics have their effects on neural synaptic and axonal activities. Hence the effect of the anesthetic on the evoked responses depends on which pathway is affected by the anesthetic and its mechanism of action, e.g., as a result from direct inhibition or indirect effects on the scale between inhibitory or excitatory inputs. The greatest decrease in amplitude and increase in latency occur in responses that are highly dependent on synaptic function, such as with inhalation anesthetics or high doses of intravenous anesthetics [74].

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At certain concentrations, inhaled anesthetics can make IOM difficult. For instance, during the recording of the MEP, the amplitude reduces in a dose-­ dependent manner with sevoflurane at the concentration for clinical use [75]. Inhaled anesthetics can cause α-wave activity in the frontal region, which can resemble sleep spindles [76]. Inhaled anesthetics affect ECoG by suppressing the spontaneous interictal spikes. Nitrous oxide (N2O) alone or in combination with sevoflurane depresses the interictal spike activity [77, 78]. Isoflurane inhibits more than propofol the IOM in spinal surgery [79]. The Voss LJ and colls’ review on seizures and general anesthetic drugs [47] followed the definitions proposed by the International League Against Epilepsy and the International Bureau for Epilepsy [80, 81]. A seizure is characterized by episodes of abnormal enhanced synchrony in neuronal activity. Therefore, the term seizure is used when the event is recorded by EEG whereas Epileptiform activity refers to small areas (60% of baseline and does not recover with tissue relaxation, postoperative nerve and vocal fold dysfunction are likely [42]. LAR amplitude decrement for warning criteria should be 50% in the brainstem and posterior fossa surgeries [48]. The difference in warning criteria between peripheral and central nervous surgery stems from sensitivity and specificity values compared in Brainstem surgery [48]. LAR interpretation during brainstem surgery is more complicated than peripheral surgery. The reader must consider the location of the brainstem and posterior fossa surgery. Particularly intraaxial brainstem surgery monitoring-related changes interpreted cautiously in case of false-positive results [38]. LAR reflex motor and sensory parts can be affected separately during intraaxial brainstem surgery; the reflex loss due to sensory central lesion may not reflect complete neurological deficit. It is advised that all functional laryngeal assessments should be done objectively, such as video laryngoscopy, not a bedside patient voice assessment.

Anesthesia and LAR R1 component can be elicited bilaterally at all depths of anesthesia in 100% of patients provided total intravenous anesthesia (TIVA) is used [42]. Previous reports investigating the LAR in humans under general anesthesia using inhalational anesthetic agents reported no discernable R2 (oligo-polysynaptic component) responses at any level of anesthesia. Although R2 components in some patients under TIVA may be present, these responses are less reliable than the R1 component and prone to fade [43]. Sometimes it is used topical lidocaine (4%) during intubation. This drug may abolish LAR and recovery could be slow, even hours. Therefore LAR monitoring necessitates avoiding Lidocaine usage altogether [44].

Practical Application LAR is a recently developed methodology in IOM and is promising to fill a significant gap for surgeries involving lower medulla and lower cranial nerves. However, the reader should understand that technical aspects of LAR methodology requires

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further refinement. Young children’s technical limitations and electrode placement have severe practical difficulties. LAR represents one of the most critical functions of the larynx, which cannot be monitored by any other methods for preventing aspiration risk.

Conclusions The brainstem reflexes are elicitable under general anesthesia, therefore opening a new door for intraoperative neuromonitoring. The evaluation of brainstem reflexes during surgery offers the opportunity to assess continuously, and in real-time, the functional integrity of all anatomical structures involved in the reflex arc since it does not produce any movement of the patient and the surgical field is not disturbed. From the IOM perspective, brainstem reflexes give us a substantial advantage to continuously monitor the integrity of the cranial nerves involved, but we should also consider the reflex function and consequences, not only general nerve functions. To conclude, the methodology to elicit brainstem reflexes is feasible and reliable, and it might be implemented in the routine of intraoperative neuromonitoring protocols.

References 1. Ambalavanar R, et al. Neuronal activation in the medulla oblongata during selective elicitation of the laryngeal adductor response. J Neurophysiol. 2004;92(5):2920–32. 2. Andreatta RD, et al. Mucosal afferents mediate laryngeal adductor responses in the cat. J Appl Physiol (1985). 2002;93(5):1622–9. 3. Barkmeier JM, et al. Modulation of laryngeal responses to superior laryngeal nerve stimulation by volitional swallowing in awake humans. J Neurophysiol. 2000;83(3):1264–72. 4. Bieger D, Hopkins DA.  Viscerotopic representation of the upper alimentary tract in the medulla oblongata in the rat: the nucleus ambiguus. J Comp Neurol. 1987;262(4):546–62. 5. Bolser DC, et al. Role of the dorsal medulla in the neurogenesis of airway protection. Pulm Pharmacol Ther. 2015;35:105–10. 6. Bricolo A, Sala F. Surgery of Brainstem lesions. Neurophysiology in Neurosurgery. A modern intraoperative approach. Academic Press; 2002. Ed Ch 12. p. 267–89. 7. Cruccu G, Truini A, Priori A.  Excitability of the human trigeminal motoneuronal pool and interactions with other brainstem reflex pathways. J Physiol. 2001;531:559–71. 8. Cruccu G, Iannetti GD, Marx JJ, Thoemke F, Truini A, Fitzek S, et al. Brainstem reflex circuits revisited. Brain. 2005;128:386–94. 9. Cruccu G, Hallet M.  Brainstem function and dysfunction. Clin Neurophysiol. (Suppl.). 2006;58:4. 10. Deletis V, Vodušek DB.  Intraoperative recording of bulbocavernosus reflex. Neurosurgery. 1997;40:88–93. 11. Deletis V, Ulkatan S, Cioni B, Meglio M, Colicchio G, Amassian V, Shrivastava R. Responses elicited in the vocalis muscles after electrical stimulation of motor speech areas. Rivista Med. 2008;14(2):159–65.

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12. Deletis V, Urriza J, Ulkatan S, Fernandez-Conejero I, Lesser J, Misita D. The feasibility of recording blink reflexes under general anesthesia. Muscle Nerve. 2009a;39(5):642–6. 13. Deletis V, Fernandez-Conejero I, Ulkatan S, Costantino P. Methodology for intraoperatively eliciting motor evoked potentials in the vocal muscles by electrical stimulation of the corticobulbar tract. Clin Neurophysiol. 2009b;120(2):336–41. 14. Deletis V, Fernández-Conejero I, Ulkatan S, Rogić M, Carbó EL, Hiltzik D.  Methodology for intra-operative recording of the corticobulbar motor evoked potentials from cricothyroid muscles. Clin Neurophysiol. 2011;122(9):1883–9. 15. Deletis V, Fernández-Conejero I. Intraoperative monitoring of the functional integrity of the brainstem. J Clin Neurol. 2016;12(3):262–73. 16. Dong CC, Macdonald DB, Akagami R, Westerberg B, Alkhani A, Kanaan I, Hassounah M. Intraoperative facial motor evoked potential monitoring with transcranial electrical stimulation during skull base surgery. Clin Neurophysiol. 2005;116(3):588–96. 17. Esteban A. A neurophysiological approach to brainstem re- flexes. Blink Reflex Neurophysiol Clin. 1999;29:7–38. 18. Fernández-Conejero I, Ulkatan S, Deletis V. Upper facial nerve motor evoked potentials can be a misinterpretation of the blink reflex. J Neurol Neurosurg Psychiatry. 2008. Letter to Editor. 19. Fernández-Conejero I, Ulkatan S, Sen C, Deletis V. Intra-operative neurophysiology during microvascular decompression for hemifacial spasm. Clin Neurophysiol. 2012;123(1):78–83. 20. Godaux E, Desmedt JE. Human masseter muscle: H- and tendon reflexes. Their paradoxical potentiation by muscle vibration. Arch Neurol. 1975;32(4):229–34. 21. Henriquez VM. Laryngeal reflex responses are not modulated during human voice and respiratory tasks. J Physiol. 2007;585(Pt.3):779–89. 22. Heitmiller RF, Tseng E, Jones B. Prevalence of aspiration and laryngeal penetration in patients with unilateral vocal fold motion impairment. Dysphagia. 2000;15(4):184–7. 23. Kanotra SP. GlideScope-assited nerve integrity monitoring tube placement for intraoperative recurrent laryngeal nerve monitoring. J Laryngol Otol. 2012;126(12):1271–3. 24. Kimura J. Electrodiagnosis in diseases of nerve and muscle: principles and practice. F.A. Davis Company; 1989. p. 361–2. 25. Kugelberg E. Facial reflexes. Brain. 1952;75:385–96. 26. Ludlow CL.  Central nervous system control of the laryngeal muscles in humans. Respir Physiol Neurobiol. 2005;147(2–3):205–22. 27. Macaluso GM, De Laat A. H-reflexes in masseter and temporalis muscles in man. Exp Brain Res. 1995;107(2):315–20. 28. Marelli RA, Hillel AD. Effects of general anesthesia on the human blink reflex. Head Neck. 1989;11:137–49. 29. Moller AR, Jannetta PJ. Hemifacial spasm: results of electro- physiologic recording during microvascular decompression operations. Neurology. 1985;35:969–74. 30. Mourisse J, Gerrits W, Lerou J, van Egmond J, Zwarts MJ, Booij L. Assessment of blink and corneal reflexes during midazolam administration: useful methods for assessing depth of anesthesia? Acta Anaesthesiol Scand. 2003;47:593–600. 31. Mourisse J, Lerou J, Zwarts M, Booij L. Electromyographic assessment of blink reflexes correlates with a clinical scale of depth of sedation/anaesthesia and BIS during propofol ad- ministration. Acta Anaesthesiol Scand. 2004;48:1174–9. 32. Mourisse J, Lerou J, Struys M, Zwarts M, Booij L.  Multi-level approach to anaesthetic effects produced by sevoflurane or propofol in humans: 1. BIS and blink reflex. Br J Anaesth. 2007;98:737–45. 33. Murakami Y, Kirchner JA. Mechanical and physiological properties of reflex laryngeal closure. Ann Otol Rhinol Laryngol. 1972;81(1):59–71. 34. Ongerboer de Visser BW. Afferent limb of the human jaw reflex: electrophysiologic and anatomic study. Neurology. 1982 May;32(5):563–6. 35. Pechstein U, Cedzich C, Nadstawek J, Schramm J.  Transcranial high-frequency repetitive electrical stimulation of recording myogenic motor evoked potential with the patient under general anesthesia. Neurosurgery. 1996;39:335–44.

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36. Rodi Z, Vodušek DB. Intraoperative monitoring of bulbocavernous reflexthe method and its problems. Clin Neurophysiol. 2001;112:879–83. 37. Sasaki CT.  Laryngeal physiology for the surgeon and clinician. San Diego, CA: Plural Publishing, Inc; 2017. p. 1. online resource (xii, 115 pages). 38. Satomaa AL, Vanttinen S, Mattila H.  The intraoperative laryngeal adductor reflex (LAR) in brainstem tumor removal: a case of unilateral loss of LAR signal. Clin Neurophysiol. 2019;130:1253–5. 39. Seymour AH, Prakash N. A cadaver study to measure the adult glottis and subglottis: defining a problem associated with the use of double-lumen tubes. J Cardiothorac Vasc Anesth. 2002;16(2):196–8. 40. Shahani B. The human blink reflex. J Neurol Neurosurg Psychiatry. 1970;33:792–800. 41. Sinclair CF, Tellez MJ, Ulkatan S. Human laryngeal sensory receptor mappingilluminates the mechanisms of laryngeal adductor reflex control. Laryngoscope. 2018a;128(11):E365–70. 42. Sinclair CF, Tellez MJ, Ulkatan S. Noninvasive, tube-based, continuous vagal nerve monitoring using the laryngeal adductor reflex: Feasibility study of 134 nerves at risk. Head Neck. 2018b;40(11):2498–506. 43. Sinclair CF, Tellez MJ, Tapia OR, Ulkatan S. Contralateral R1 and R2 components of the laryngeal adductor reflex in humans under general anestehsia. Laryngoscope. 2017a;127(12):443–8. 44. Sinclair CF, Tellez MJ, Ulkatan S. A novel methodology for assessing laryngeal and vagus nerve integrity in patients under general anesthesia. Clin Neurophysiol. 2017b;128(7):1399–405. 45. Steriade M, McCarley RW, SpringerLink (Online service). Brain control of wakefulness and sleep. New York, NY/Boston, MA: Kluwer Academic/Plenum Publishers; 2005. 46. Szentagothai J.  Anatomical considerations on monosynaptic reflex arcs. J Neurophysiol. 1948;11(5):445–54. 47. Tellez MJ, Ulktana S, Blitzer A, Sinclair CF. Unearthing a consistent bilateral R1 component of the laryngeal adductor reflex in awake humans. Laryngoscope. 2018;128(11):2581–7. 48. Tellez MJ, Mirallave-Pescador A, Seidel K, Urriza J, Shoakazemi A, Raabe A, Ghatan S, Deletis V, Ulkatan S. Neurophysiological monitoring of the laryngeal adductor refle during cerebellar-pontine angle and brainstem surgery. Clin Neurophysiol. 2021. 49. Ulkatan S, Jaramillo AM, Téllez MJ, Goodman RR, Deletis V.  Feasibility of eliciting the H reflex in the masseter muscle in patients under general anesthesia. Clin Neurophysiol. 2017;128(1):123–7. 50. Valls-Solé J. Neurophysiological assessment of trigeminal nerve reflexes in disorders of central and peripheral nervous system. Clin Neurophysiol. 2005;116(10):2255–65.

Part III

Brain Functions: Eloquent Areas

Chapter 13

The Brain Surface Eduardo Carvalhal Ribas and Guilherme Carvalhal Ribas

Introduction The encephalon is the part of the central nervous system that lies within the intracranial space. It is divided by the tentorium into an infratentorial compartment, which contains the brainstem and cerebellum, and a supratentorial compartment, which contains the diencephalon and the telencephalon constituted by two cerebral hemispheres separated by the falx. In order to favor its better understanding, organize its nomenclature, and apply this knowledge in clinical practice, the cerebral hemispheres were arbitrarily divided into lobes, regions, and compartments. As these divisions correspond to different concepts and have been created according to different criteria, they partly overlap, are complementary to each other, and are particularly useful for a better understanding of the brain architecture [1]. Among other criteria, the brain can be subdivided according to its sulcal patterns, comparative anatomy, cytoarchitecture, myeloarchitecture, myelogenesis, connectivity, and cerebral functions. The mean volume of the brain ranges between 440 and 517 cm3 (females and males, respectively), weighting 1508.91  ±  299.14  g and housing 170.68  ±  13.86 cells, where half are neuronal cells (Table 13.1) [2]. The surface of the brain, also called cortex, is much larger than that of a simple ovoid structure. Due to its convoluted shape, almost two thirds of the human neocortex are hidden away in the depth of the sulci, ranging in total between 1470 and 2275 cm2.

E. C. Ribas (*) · G. C. Ribas Hospital Israelita Albert Einstein, São Paulo, SP, Brazil University of São Paulo Medical School, São Paulo, SP, Brazil © The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 S. M. Verst et al. (eds.), Intraoperative Monitoring, https://doi.org/10.1007/978-3-030-95730-8_13

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Table 13.1  The number of neuronal and nonneuronal cells of the brain [2]

Mass (g) All cells (billions) Neuronal cells (billions) Nonneuronal cells (billions) Nonneuronal/ neuronal cells ratio Percentage of brain mass Percentage of brain neurons

Telencephalon (gray and white matters) Whole brain 1508.91 ± 299.14 1232.93 ± 233.68 170.68 ± 13.86 77.18 ± 7.72

Basal ganglia, diencephalon, mesencephalon, and pons Cerebellum 154.02 ± 19.29 17.66 ± 45.42 85.08 ± 6.92 8.42 ± 1.50

86.06 ± 8.12

16.34 ± 2.17

69.03 ± 6.65

0.69 ± 0.12

84.61 ± 9.83

60.84 ± 7.02

16.04 ± 2.17

7.73 ± 1.45

0.99

3.76

0.23

11.35

100%

81.8%

10.3%

7.8%

100%

19.0%

80.2%

0.8%

Sulcal Pattern The phylogenetic and embryological development of the brain surface is based on its invagination processes, being the fissures and sulci natural extensions of the subarachnoid space, with depths ranging from 1 to 3 cm approximately and harboring small gyri within its sulcal space, known generically as transverse gyri [3]. Also, the brain undergoes a process of circular curvature, placing each thalamus as the morphological center of each cerebral hemisphere. These processes led to a typical superficial organization of sulci and gyri. Each mammalian species has a highly characteristic cerebral surface, with humans having a higher complexity. However, there’s a considerable intersubject variability if individual sulci are seen in detail. Sulci may be continuous or interrupted, once or at several points, and some sulci may be doubled over a certain part of their trajectory [4]. The sulcal pattern not only varies among individuals but also varies between the two hemispheres of the same individual. The cerebral gyri constitute a continuum of the cerebral surface, and their appearance as distinct gyri is only superficial since they are continuous along the entire sulcal depth and along its extremities. Also, in humans, almost two thirds of the neocortex are hidden away in the depth of the sulci [5]. Therefore, each gyrus must be understood as a region and not as a well-defined and distinct structure [6]. Currently, the International Anatomical Terminology describes each cerebral hemisphere as being divided into six lobes: frontal, parietal, occipital, temporal, insular, and limbic [7]. The lateral sulcus of the brain, also called the Sylvian fissure, is promptly and easily identifiable. It has a stem, which extends from the carotid cistern to the

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anterior Sylvian point on the superolateral surface of the brain, and gives rise to three rami: anterior horizontal, anterior ascending, and posterior [8]. The anterior horizontal and anterior ascending rami delineates the pars triangularis in the inferior frontal gyrus, having the pars orbitalis anterior to the anterior horizontal ramus and the pars opercularis posterior to the anterior ascending ramus. The posterior ramus separates the frontal and parietal lobes superiorly from the temporal lobe inferiorly. The parietotemporal line is an imaginary line, drawn from the upper extremity of the parieto-occipital sulcus on the lateral surface to the preoccipital notch, and constitutes the anterior limit of the occipital lobe. Another imaginary line, drawn as a posterior continuation of the Sylvian fissure to the parietotemporal line, separates the parietal lobe superiorly from the temporal lobe inferiorly. The insula is separated from the other cerebral lobes by its anterior, superior, and inferior limiting sulci; and the limbic lobe is bounded by the cingulate and collateral sulci [9]. Each cerebral hemisphere has three surfaces: superolateral, medial, and basal; three margins: superior, inferior, and medial; and three poles: frontal, temporal, and occipital. The superolateral surface of the brain, also referred to as cerebral convexity, faces the concave inner surface of the skull (Fig. 13.1a). At this surface, three horizontal gyri (superior, middle, and lower frontal gyri) converge anteriorly to form the frontal pole, three horizontal gyri (upper, middle, and inferior temporal gyri) converge anteriorly to form the temporal pole, and three gyri (superior, middle, and inferior occipital gyri) converge posteriorly to form the occipital pole. Two oblique, ascending gyri are clearly seen: precentral and postcentral gyri. Immediately posteriorly, a quadrangular region called the superior parietal lobule can be noted superiorly, and the inferior parietal lobule inferiorly, formed by two curved gyri: the supramarginal gyrus, which can be seen as the posterior continuation of the superior temporal gyrus and whose trajectory curves over the posterior margin of the Sylvian fissure; and the angular gyrus, which corresponds to a posterior and curvilinear extension of the middle temporal gyrus forming a horse-shoe “C” shape [6]. Although a considerable intersubject variability exists, some uniformity can be noted. The superior frontal and superior temporal sulci are usually continuous, whereas the inferior frontal and inferior temporal sulci are usually interrupted. The pre- and postcentral sulci are always interrupted: the first having interruptions due to the frontal gyri connections to the precentral gyrus and the second having interruptions due to the postcentral gyrus connections with the superior parietal lobule. The intraparietal sulcus separates the superior and inferior parietal lobules and is usually clearly identifiable with an anterior-posterior disposition. The intermediate sulcus of Jensen is located between the supramarginal and angular gyri, and can arise from the intraparietal sulcus, superior temporal sulcus, or both. The occipital gyri have a higher intersubject variability. The medial surface of the brain lies at the depth of the interhemispheric fissure, where both hemispheres face each other, and is anatomically more constant (Fig. 13.1b). The corpus callosum is placed around its inferior margin with the cingulate gyrus describing an arc around it. Anteriorly and inferiorly, the cingulate

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a

c

b

d

Fig. 13.1  Cortical anatomy of the brain: lateral (a), medial (b), basal (c), and insular (d) surfaces. AcG accessory gyrus, ALS anterior limiting sulcus, AngG angular gyrus, CalcF calcarine fissure, CaS callosal sulcus, CC corpus callosum, CerHem cerebellar vermis, Ch optic chiasm, CiG cingulate gyrus, CiIst cingulate isthmus, CiMR cingulate marginal ramus, CiS cingulate sulcus, ColS collateral sulcus, CS central sulcus, Cu cuneus, For fornix, FusG fusiform gyrus, IFG inferior frontal gyrus, IFS inferior frontal sulcus, III third ventricle, ILS inferior limiting Sulcus, InsCS insular central sulcus, IntS intermediate sulcus of Jensen, IOG inferior occipital gyrus, IOS inferior occipital sulcus, IPS intraparietal sulcus, IRS inferior rostral sulcus, ITG inferior occipital gyrus, ITG inferior temporal gyrus, ITS inferior temporal sulcus, IV fourth ventricle, LatVen lateral ventricle, LiG lingual gyrus, LInsG long insular gyri, LInsG long insular gyrus, Med medulla oblongata, MFG middle frontal gyrus, Mid midbrain, MOG middle occipital gyrus, MTG middle temporal gyrus, OffS olfactory sulcus, OlfTr olfactory tract, OrbG orbital gyri, OrbS orbital sulcus, OTS occipito-temporal sulcus, ParaCL paracentral lobule, ParaCS paracentral sulcus, ParaHipG parahippocampal gyrus, POF parieto-occipital fissure, PostCG postcentral gyrus, PostCS postcentral sulcus, PreCG precentral gyrus, PreCS precentral sulcus, PreCu precuneus, RG rectus gyrus, RinS rinal sulcus, SFG superior frontal gyrus, SFS superior frontal sulcus, SInsG short insular gyri, SLS superior limiting sulcus, SOG superior occipital gyrus, SOS superior occipital sulcus, SPL superior parietal lobule, SRS superior rostral sulcus, STG superior temporal gyrus, STS superior temporal sulcus, SupraMG supramarginal gyrus, SyFi sylvian fissure, TransG transverse gyrus, Ver cerebellar vermis

gyrus joins the rectus gyrus forming the cingulate pole. The rectus gyrus harbors the inferior rostral sulcus and is separated from the superior frontal gyrus by the superior rostral gyrus. Three vertical gyri can be identified posterior to the cingulate pole and form the septal region: anterior para-olfactory gyrus, posterior para-olfactory

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gyrus, and paraterminal gyrus. Posteriorly, the cingulate gyrus presents a narrowing, called the isthmus, which continues with the parahippocampal gyrus. The superior frontal gyrus curves along the superior cerebral margin, and along the medial surface of brain, it is separated from the cingulate gyrus by the cingulate sulcus. Similarly, the precentral and postcentral gyri also curve along the superior cerebral margin and along the medial surface of brain form together the paracentral lobule. The cingulate sulcus separates the paracentral lobule inferiorly from the cingulate gyrus, and posteriorly curves superiorly to constitute the ascending ramus of the cingulate sulcus separating the paracentral lobule from the pre-cuneus. The paracentral sulcus originates more anteriorly from the cingulate sulcus and separates the superior frontal gyrus from the paracentral lobule. The precuneus has a quadrangular shape, is incompletely separated inferiorly from the cingulate gyrus by the subparietal sulcus rami, and is deeply separated anteriorly from the paracentral lobule by the ascending ramus of the cingulate sulcus and posteriorly from the cuneus by the parieto-occipital fissure. The cuneus has a triangular shape, with its vertex pointing anteriorly, and is separated from the lingual gyrus by the calcarine fissure. The calcarine fissure is divided into two parts by the origin of the parieto-­ occipital sulcus. While the proximal part supports the isthmus where it is originated and the caudal base of the precuneus, the distal part lies between the cuneus and the lingual gyrus. The basal surface of the brain lies along the base of the skull (Fig. 13.1c). The anterior fossa supports the fronto-orbital surface, constituted laterally by the orbital gyri (subdivided by the “H”-shaped orbital sulcus into anterior, posterior, lateral, and medial orbital gyri) and medially by the rectus gyrus. The temporo-occipital surface lies over the middle fossa and the tentorium, constituted by three longitudinal gyral strips: (1) laterally is the inferior temporal gyrus that continues posteriorly with the inferior occipital gyrus; (2) medially is the parahippocampal gyrus, which anteriorly curves over itself forming the uncus and posteriorly continues with both the cingulate and lingual gyri; (3) and in between there is the fusiform gyrus. The superior and medial surface of the parahippocampal gyrus, called subiculum, is flat and supports the inferior aspect and pulvinar of the thalamus. This surface is separated laterally by the hippocampal fissure from the dentated gyri, which continues posteriorly as the fasciolar gyri (also known as fasciola cinerea, gyrus of Andreas Retzius, or retrosplenial gyri) circling the splenium, and subsequently as the indusium griseum over the trunk of the corpus callosum. The indusium griseum extends also along the genu and rostrum of the corpus callosum, and finishes within the paraterminal gyrus at the septal region. The surface of the insula has a triangular shape, with the limen insulae at its anteroinferior vertex, and is separated from the other cerebral lobes by its anterior, superior, and inferior limiting sulci (Fig. 13.1d). It is subdivided by the central sulcus of the insula into an anterior portion, composed of short gyri which usually converge to form an apex, and a posterior portion, formed by long insular gyri. At its anterior and basal aspect, a transverse gyrus can be identified immediately superior to the limen insulae and an accessory gyrus can be identified superiorly to the later [1, 9].

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The disposition and arrangement of cerebral lobes can also be understood in relation to the central core of the brain [1]. The concept of central core of the brain is based on the evident anatomical delimitation of a central region within each hemisphere between the brainstem, the ventricular cavities, and the cerebral lobes, and which has important clinical and surgical implications. It is basically composed by the insular surface, basal ganglia, and thalamus, and is connected with the rest of the supratentorial compartment by cerebral isthmi (represented by the continuation of the internal, external, and extreme capsules toward the cerebral lobes). It also houses part of the anterior commissure, amygdalofugal pathways, and the region of the innominate substance. This block is at the morphological center of each cerebral hemisphere and plays an important role in the integration of information, motor and sensory functions, emotion, and cognition. From an anatomical and architectural point of view, the central core is covered laterally by the insula, medially by the supratentorial ventricular surfaces, and embraced by the limbic lobe which describes a “C”-shaped ring around the thalamus. The frontal, parietal, occipital, and temporal lobes are placed anteriorly, superiorly, posteriorly, and inferiorly in relation to the central core, respectively. Detailed knowledge of the cerebral surface, formed by sulci and turns, is essential for the interpretation of imaging exams and intraoperative guidance. Once identified, the cerebral sulci can be used by the neurosurgeon as landmarks, as microneurosurgical corridors, and also as an aid for cortical mapping techniques in order to identify specific sites related to cortical functions. Although the sulci and the gyri of the brain are easily identified in standard magnetic ressonance images, their accurate visual transoperative recognition is notoriously difficult because of their common anatomic variations and their arachnoid, cerebrospinal fluid, and vessel coverings. Ribas et al. studied sulcal and gyral key points with more constant anatomical cranial-cerebral relationships, mostly formed by the main sulci extremities and/or intersections, and by the gyral sites that underlie particularly prominent cranial points (Fig. 13.2) [8, 10, 11]. These key points together constitute a neurosurgical anatomic framework that can help in the understanding of other cerebral sulci, lesions, and that can be used to orient the placement of supratentorial craniotomies and to ease the initial transoperative identification of

Superior Frontal Sulcus/ Precentral Sulcus Meeting Point x Posterior Coronal Point

Superior Rolandic Point x Superior Sagittal Point

Inferior Frontal Sulcus / Precentral sulcus meeting point x Stephanion

The Intraparietal Sulcus / Postcentral Sulcus Meeting Point x Intraparietal Point

Anterior Sylvian Point x Anterior Squamous Point

Supramarginal Gyrus x Euryon

Inferior Rolandic Point x Superior Squamous Point

External Occipital Fissure depth of the Parieto-Occipital Sulcus x Lambdoid/Sagittal Point

Posterior Extremity of the Superior Temporal Sulcus x Temporoparietal Point

Distal End of the Calcarine Fissure x Opisthocranion

Fig. 13.2  Main and gyral key points. (Adapted from Ribas et al. [6])

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b

Fig. 13.3  Van Essen’s flat maps of the left human cerebral hemisphere surface. (a) The sulcal surfaces are shaded in gray and the main sulci are labelled. In order to facilitate orientation, the structures visible at a lateral surface of the hemisphere are present between the red lines, and the medial and basal surfaces are outside the red lines. If the dashed, arrow-headed curves are connected at corresponding points, the flat map can be transformed into a tri-dimensional map. (b) The cytoarchitectonic areas of Brodmann can be transferred and depicted onto these flat maps. (Adapted from Drury and Van Essen et al. [12, 13])

brain sulci and gyri. Anatomical landmarks can be used as complementary, and not substitute, stereotactic, and navigation systems when available; and transoperative functional or neurophysiological testing is paramount for eloquent cerebral areas identification. The “folded” natural surface of the brain buries vast neocortical areas, with two thirds of the neocortex present in the depth of the sulci, and can be a barrier to researches focused on the cortical surface. To address this problem, Van Essen et al. used computerized transformations to “unfold” the entire surface of a cerebral hemisphere into a two-dimensional reconstruction or flat map, where all cortical surface can be represented (Fig.  13.3) [12]. Other cortical information, like Brodmann’s areas, can be transferred and depicted onto these flat maps.

Cytoarchitecture The cerebral cortex is recognized as a laminated structure throughout its extent by using these staining methods. The piriform cortex and hippocampal parts of the paleomammalian cortex have three layers of cells, known as allocortex or paleocortex. The neocortex, also designated as isocortex or homogenetic cortex, represents the vast majority of the cortical area and is formed by six layers of cells, which are (beginning at the surface): I. Lamina molecularis (or lamina zonalis), made by sparsely scattered horizontal cells of Cajal and the horizontal fibers of pyramidal cells, stellate cells, and cells of Martinotti.

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II. Lamina granularis externa, composed of small, densely packed stellate and small pyramidal cells. This area is traversed by vertical fibers from both ascending axons and apical dendrites of large pyramidal cells in lamina V. The ascending axons often synapse with the apical dendrites in this layer. III. Lamina pyramidalis externa, a thick layer with high pyramidal somata relation and neurons increasing progressively in size from superficial to deep. IV. Lamina granularis interna, made by small, densely packed, pyramidal, and non-­ pyramidal somata. V. Lamina pyramidalis interna, constituted mainly by medium-sized and large, loosely arranged pyramidal somata. It is also characterized by many ascending and descending fibers. A horizontal band of concentrated fibers, the internal band of Baillarger, traverses this layer. VI. Lamina multiformis, composed of relatively tightly packed, spindle-shaped somata of a variety of morphological type. The basic laminar pattern is seen at the entire neocortex, but it is not a homogeneous structure. Korbinian Brodmann distinguished 44 sharply delineated areas, although his images show areas numbered up to 52, the areas numbered 13–16, and 48–51 are not shown (Fig. 13.4) [14–16]. Von Economo and Koskinas and Sarkissov distinguished more areas, subdividing several of Brodmann’s areas (BA) into smaller ones [13]. Distinct inputs reach the cortex, and each is directed to a different cortical layer: • Layer I: inputs from intralaminar thalamic nuclei, the reticular formation, and feedback from precursor cortical areas. • Layers II and IV: intrinsic inputs from the same cortical unit. • Layers II, III, and IV: feedforward inputs from adjacent cortical regions. • Layers III and IV: thalamic and commissural inputs. • Layers V and VI: intrinsic and some thalamic inputs. Information in layer I is transferred to the intrinsic circuitry of the cortical unit by providing afferent contacts with the apical dendrites of supragranular (layers II and III) and infragranular neurons (layers V and VI). Layers II and IV provide information to the supragranular and infragranular neurons within a cortical module [17]. Efferent fibers arise from the cortical neurons and form three distinct categories: (1) the association fibers, (2) the striatal fibers, and (3) the confluence of fibers (the “cord”) that carries the commissural and subcortical fibers. Layers II and III give rise to association and commissural systems, while layers V and VI to subcortical connections. The short association fibers (aka local or U-fibers) are found directly underneath the sixth layer. Neighborhood and long association fibers travel within the central part of the white matter of the core of the gyrus, accompanied in the initial stages by the striatal fibers. The subcortically directed fibers and the commissural fibers travel initially centripetally in the central part of the white matter of the gyrus and form a “cord” formation. These fibers segregate later into commissural fibers and the subcortical bundle, which further divides into fibers destined for thalamus, and those to brainstem and spinal cord in the pontine bundle [17].

13  The Brain Surface Fig. 13.4 “Cytoarchitectonic cortical areas after Brodmann” (a, b), as mentioned in the final and modified version of the Brodmann’s cortical map, and Brodmann’s only map of the insular and adjacent supratemporal cortex (c) [16]

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Intrinsic Connectivity Broadly, brain intrinsic connections are separated in thalamocortical and cortico-­ cortical groups, and distinct areas are related with different connections.

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Fig. 13.5 Connections between the thalamic nuclei and the cerebral cortex II: cortical projection areas of the thalamic nuclei. AT anterior thalamic nuclei, CM centromedian nucleus, LGB lateral geniculate body, LP lateral posterior nucleus, MD mediodorsal thalamic nucleus, MGB medial geniculate body, PF parafascicular nucleus, Pulv (ant) pulvinar thalami, anterior part, Pulv (lat) pulvinar thalami, lateral part, Pulv (med) pulvinar thalami, medial part, VA ventral anterior thalamic nucleus, VL ventral lateral nucleus, VMP ventromedial posterior nucleus, VPC ventral posterior complex. (Adapted from Nieuwenhuys et al. [13])

The entire cortex receives thalamic projections, which arise from four main groups of thalamic nuclei (sensory relay, motor relay, limbic, and association nuclei) (Fig. 13.5). The cortico-cortical connections will spread information from primary areas to association areas. Each primary sensory area is adjoined by a modality-specific sensory association area: somatosensory unimodal association cortex (SA) is located directly behind the primary somatosensory area (BA 3, 1 and 2) and include parts of BA 5 and 7 (at the superior parietal lobule) and parts of BA 40 (at the inferior parietal lobule); visual unimodal association cortex (VA) extends over the occipital lobe and anteriorly into the temporal lobe posterior aspect, including BA 18, 19, 20, 21, and 37; and auditory unimodal association cortex (AA) is around the primary auditory cortex (located in Heschl’s gyrus, corresponding BA 41 and 42), and includes the superior temporal gyrus (BA 22). Some areas in the posterior orbitolateral cortex and anterior insula may correspond to the olfactory unimodal association area. Marek-Marsel Mesulam considers the premotor cortex (BA 6, 8, and 44), located anterior to the primary motor, a motor association area (MA), a motor analogue of

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the modality-specific sensory association areas because it provides the main cortical input to this region. Human brains have 3 heteromodal association areas (polymodal or supramodal areas), which receive inputs from unimodal areas, other heteromodal areas, and paralimbic areas. A parietotemporal heteromodal association area is located at the superior parietal lobule inferior aspect (BA 7), inferior parietal lobule (BA 39 and 40), and anteriorly into the temporal lobe (BA 21 and 22); a medial temporal heteromodal association area is seen at the perirhinal areas (BA 35 and 36); and a prefrontal heteromodal association area located anterior to the motor association cortex (BA 9, 10, 45, 46, 47 and the anterior aspects of BA 8, 11, and 1).

Cerebral Functions Several theories and models have been proposed to explain the functional organization of the brain, and can usually be classified into three different concepts: equipotentiality, localizationism, and connectionism. For historic purposes, interesting to point that the equipotentially theory, or anti-­ localizationism, believed that the entire brain, or at least one complete hemisphere, is implied in the practice of a functional task. Localizationism, on the other hand, states that each region of the neocortex is related to complete and distinct function. Franz Joseph Gall (1758–1828) and his collaborator Johann Spurzheim (1758–1832) were pioneers in this concept founding phrenology. The connectionism theory, or disconnectionism, includes the idea of functional specialized areas, but understands that cognitive functions are best explained as a result from the functional integration of the elementary processing operations occurring in different functional areas, which are interconnected by networks. Also, the traditional view of brain composed of fixed “eloquent” and “non-­ eloquent” regions, used respectively to define the regions whose lesion gives rise to major irrevocable neurological deficits and to the regions which lesions would not cause clinical consequences, is challenged by this connectivist view of brain functions. The dogma of a static functional organization of the brain which would not be able to compensate any injury involving these so-called eloquent areas is criticized by the connectivist view by considering cerebral plasticity. The phenomenon of cerebral plasticity which allows cerebral functions remodeling through the recruitment of other preserved cerebral networks constitutes both the basics and the main clinical contribution of this connectivist view. Marek-Marsel Mesulam postulated that five anatomically defined large-scale networks are most relevant to clinical practice: left-dominant perisylvian network for language, a right-dominant parietofrontal network for spatial cognition, an occipitotemporal network for face and object recognition, a limbic network for retentive memory, and a prefrontal network for attention and behavior. The inner organization of networks may vary from one person to another (as in the case of

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right versus left handers) and may therefore need to be ascertained individually when the goal is to guide surgical interventions [18, 19]. Functional magnetic resonance imaging (fMRI) and positron emission tomography (PET) are recent advances in functional neuroimaging methods that can detect changes in blood flow or metabolism in specific regions of the brain while human subjects perform various sensory, motor, or cognitive tasks (Fig.  13.6). Since increased blood flow and metabolism reflect changes in neuronal activity, particularly synaptic, these methods can identify which cortical areas are more functionally a

b

Fig. 13.6  Summary of activation cortical areas from functional imaging experiments, depicted upon the lateral (a) and medial (b) surface of the brain. a: attention, b: calculation, c: activation arising from a working memory task, d: processing of incorrect arithmetic equations, e: maternal love, f: performance of a verbal working memory task, g: reading aloud irregular words, h: meditative state, j: finger opposition task, k: visual-spatial orienting, l: coherence processes in language comprehension, m: executive function in working memory, n: embarrassment, o: perception of visual motion, p: written sentence comprehension, q: processing of color patterns, r: verb comprehension, s: judgment of the grammaticality of sentences, t: selective auditory attention, u: evaluation of unpleasant, arousing words, v: cross-modal sensory processing, w: error processing, x: categorization of written object descriptions, y: pursuit eye movements, z: painful visceral sensation, a1: saccades, b1: visual stimulation. (From Nieuwenhuys et al. [13])

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activated during a given brain function. Cortical functional maps based on neuroimaging methods can help in clinical practice to highlight cortical areas related to each brain function, but cannot infer which areas are essential or critical for performing a specific brain function. Diffusion-weighted imaging (DWI) is a modern MRI technique that can measure the thermal Brownian motion of water molecules and diffusion tensor imaging (DTI) can also detect the more favorable diffusivity direction of these molecules, termed anisotropy. Since water molecules tend to diffuse more freely along the direction of axonal fascicles rather than across them at the subcortical space, tracking and tracing the more favorable trajectory of water molecules allows the 3D reconstruction of white matter tracts, a technique called fiber tractography (FT). The white matter tracts architectural arrangement can now be studied in vivo and individually; however, fiber tractography can still not inform about the function and eloquency of a given tract. Brain mapping techniques using direct electric stimuli on cortical areas and subcortical white matter are seen as the gold standard for clarifying the function and eloquency of each region and have brought us new insights about the anatomo-­ funcional organization of the brain. More recently, Hugues Duffau, who has worked extensively with brain mapping during awake neurosurgeries with patients affected by gliomas, has contributed enormously by identifying cortical areas and subcortical pathways related to different brain functions. Presurgical understanding of the basic anatomo-functional organization of the brain is crucial to optimize the selection of the most appropriate intraoperative tasks for the patient, given the limited intrasurgical awake time frame. An ideal intraoperative protocol includes essential tasks related to the function of each cerebral region and additional tests that can be chosen on the basis of each patient-specific profile, in order to preserve an optimal quality of life [20]. Duffau et al. also proposed the concept of a “minimal common brain,” which is based in connectivism at the expense of cortical localizationism (Fig. 13.7). This work brings a probabilistic postsurgical tumor residue atlas computed on a series of patients who underwent incomplete WHO grade II glioma resection on the basis of intraoperative direct electric stimuli brain mapping, and suggests which cortical areas and subcortical pathways are essential for the basic cognitive functions despite the inter-individual anatomo-functional variability and plastic mechanisms. By relating the high probability of residual tumor to regions in the deep white matter, projection and association axonal pathways seem to play a critical role in the proper functioning of the brain. The functions subserved by long-range axonal pathways seem to be less subject to inter-individual variability and reorganization than cortical sites, and constitute the main obstacle to radical tumor surgical resection. Input and output areas, being respectively the first relay of information entering the brain and the last relay or the fiber tracts sending information, have to be preserved probably due to absence of parallel alternative pathways to restore their function after any damage; examples are projection fibers, primary motor and somatosensory areas. Other essential areas may act as with cortical epicenters or “hubs,” connected by U-shaped fibers, associative and commissural pathways, required to allow proper

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Supplementary motor area

Motor areas of hand

Z= 45

Z= 30 Broca area Right hemisphere homologous of Broca area

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Fig. 13.7  Probabilities of residual WHO grade II glioma after resection under brain mapping (residual tumor index). (From Ius et al. [21])

synchronization between several distant areas or to integrate plurimodal data coming from the unimodal areas, like the posterior part of the left dominant superior temporal gyrus and its junction with the inferior parietal lobule [21].

Multi-modal Parcellation More recently, researches have used high-quality magnetic resonance imaging (MRI) data provided by the Human Connectome Project, which benefited from major advances in image acquisition and preprocessing, to parcellate cerebral cortical regions by combining cortical architecture, function, connectivity, and/or topography together. Architectural measures of relative cortical myelin content and cortical thickness were derived from T1-weighted and T2-weighted structural images; cortical function was measured using task functional MRI contrasts from seven tasks; functional connectivity and topographic organization were analyzed from resting-state functional MRI (Fig. 13.8) [22, 23]. An objective semi-automated neuroanatomical approach was able to delineate 180 areas per hemisphere, bounded by sharp margins. Interestingly, this method characterized 97 new areas in addition to the 83 areas previously reported using

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Fig. 13.8  The Human Connectome Project’s multi-modal parcellation map, version 1.0. The 180 areas delineated and identified in both left and right hemispheres are displayed on inflated and flattened cortical surfaces. Black outlines indicate areal borders. Colors indicate the extent to which the areas are associated in the resting state with auditory (red), somatosensory (green), visual (blue), task positive (towards white), or task negative (towards black) groups of areas. (Adapted from Glasser et al. [23])

post-mortem microscopy or other specialized methods and could be replicated and validated in other group of subjects [23]. Functionally, less than half of the neocortical sheet appears to be occupied by predominantly unimodal regions, which are divided into five specialized groups of areas. Three are related to the major input streams to the brain (early auditory, early somatosensory/motor, and early visual areas), and two are core groups of cognitive areas (positive network and task negative network, also called the default mode network). Most of the cortex houses bi-modal or multi-modal areas and both hemispheres have a remarkable bilateral functional symmetry, with asymmetries most associated to language-related areas.

References 1. Ribas EC, Yağmurlu K, de Oliveira E, Ribas GC, Rhoton A. Microsurgical anatomy of the central core of the brain. J Neurosurg. 2018;129(3):752–69. 2. Azevedo FAC, Carvalho LRB, Grinberg LT, Farfel JM, Ferretti REL, Leite REP, et al. Equal numbers of neuronal and nonneuronal cells make the human brain an isometrically scaled-up primate brain. J Comp Neurol. 2009;513(5):532–41. 3. Ribas GC. The cerebral sulci and gyri. Neurosurg Focus. 2010;28(2):E2.

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4. Ono M, Kubik S, Abernathey CD. Atlas of the cerebral sulci. Stuttgart/New York: G. Thieme Verlag/Thieme Medical Publishers; 1990. 218 p. 5. Braak H.  Architectonics of the human telencephalic cortex [Internet]. Berlin, Heidelberg: Springer Berlin Heidelberg; 1980 [cited 2021 Jul 13]. Available from: https://doi. org/10.1007/978-­3-­642-­81522-­5. 6. Ribas G.  Applied cranial-cerebral anatomy: brain architecture and anatomically oriented microneurosurgery. Cambridge, UK\New York, NY: Cambridge University Press; 2018. 132 p. 7. de Anatomia SB, de Terminologia Anatômica C, da Terminologia Anatômica CF. Terminologia anatômica: terminologia anatômica internacional. São Paulo: Manole; 2001. 8. Ribas GC, Ribas EC, Rodrigues CJ. The anterior sylvian point and the suprasylvian operculum. Neurosurg Focus. 2005;18(6B):E2. 9. Ribas EC, Yagmurlu K, Wen HT, Rhoton AL. Microsurgical anatomy of the inferior limiting insular sulcus and the temporal stem. J Neurosurg. 2015;122(6):1263–73. 10. Ribas GC, Yasuda A, Ribas EC, Nishikuni K, Rodrigues AJ. Surgical anatomy of microneurosurgical sulcal key points. Neurosurgery. 2006;59(4 Suppl 2):ONS177–210; discussion ONS210–211. 11. Ribas GC, Rodrigues AJJ. The suprapetrosal craniotomy. J Neurosurg. 2007;106(3):449–54. 12. Drury HA, Van Essen DC, Anderson CH, Lee CW, Coogan TA, Lewis JW.  Computerized mappings of the cerebral cortex: a multiresolution flattening method and a surface-based coordinate system. J Cogn Neurosci. 1996;8(1):1–28. 13. Nieuwenhuys R, Voogd J, van Huijzen C.  The human central nervous system. 4th ed. New York: Springer; 2008. p. 967. 14. Brodmann K.  Feinere Anatomie des Grosshirns. In: Handbuch der Neurologie, 1 Band: Allgemeine Neurologie. Verlag von Julius Springer, Berlin: Lewandowsky, M.; 1910. 15. Brodmann K. Physiologie des Gehirns. In: Neue Deutsche Chirurgie, 11 Band: Allgemeine Chirurgie der Gehirnkrankheiten. Verlag von Ferdinand Enke, Stuttgart: Von Bruns P; 1914. 16. Judaš M, Cepanec M, Sedmak G.  Brodmann’s map of the human cerebral cortex  — or Brodmann’s maps? Transl Neurosci [Internet]. 2012 [cited 2021 Jul 31];3(1). Available from: https://www.degruyter.com/document/doi/10.2478/s13380-­012-­0009-­x/html 17. Schmahmann JD, Pandya DN.  Fiber pathways of the brain. Oxford/New York: Oxford University Press; 2006. 654 p. 18. Mesulam MM. Large-scale neurocognitive networks and distributed processing for attention, language, and memory. Ann Neurol. 1990;28(5):597–613. 19. Duffau H, editor. Brain mapping: from neural basis of cognition to surgical applications. Wien/ New York: Springer; 2011. 392 p. 20. Coello AF, Moritz-Gasser S, Martino J, Martinoni M, Matsuda R, Duffau H.  Selection of intraoperative tasks for awake mapping based on relationships between tumor location and functional networks: a review. JNS. 2013;119(6):1380–94. 21. Ius T, Angelini E, Thiebaut de Schotten M, Mandonnet E, Duffau H. Evidence for potentials and limitations of brain plasticity using an atlas of functional resectability of WHO grade II gliomas: towards a “minimal common brain”. NeuroImage. 2011;56(3):992–1000. 22. Van Essen DC, Smith SM, Barch DM, Behrens TEJ, Yacoub E, Ugurbil K, et al. The WU-Minn human connectome project: an overview. NeuroImage. 2013;80:62–79. 23. Glasser MF, Coalson TS, Robinson EC, Hacker CD, Harwell J, Yacoub E, et al. A multi-modal parcellation of human cerebral cortex. Nature. 2016;536(7615):171–8.

Chapter 14

Brain Functions: Eloquent Areas – Motor and Somatosensory Kathleen Seidel and Marcos Vinicius Calfat Maldaun

Abbreviations CST DCS GTR M1 MEP TES

Corticospinal tract Direct cortical stimulation Gross total resection Primary motor area Motor evoked potential Transcranial electrical stimulation

The Neuro-oncological Challenge Minimizing the risk of disabling motor deficits is a main factor during surgery in eloquent motor areas. At the same time, this constitutes the major challenge for the neurosurgeon, who aims to achieve the best possible surgical outcome, such as maximal extent of tumor removal, without compromising the patient’s functional status. Complete removal or gross total resection (GTR) remains the surgical goal for most intracranial tumors including gliomas, and there is increasing evidence that GTR prolongs overall and progression-free survival in lower grade gliomas and K. Seidel (*) Department of Neurosurgery, Inselspital, Bern University Hospital, University of Bern, Bern, Switzerland e-mail: [email protected] M. V. C. Maldaun Instituto de Ensino e Pesquisa (Teaching and Research Institute) of Hospital Sirio Libanês, São Paulo, SP, Brazil Neurosurgery Department, Hospital Sirio Libanês, São Paulo, São Paulo, Brazil © The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 S. M. Verst et al. (eds.), Intraoperative Monitoring, https://doi.org/10.1007/978-3-030-95730-8_14

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glioblastomas [1–7]. However, more than 50% of these tumors are judged to be “presumably eloquent” based on the preoperative images [8–10]. Intraoperative neurophysiological mapping can help to verify or falsify intraoperative eloquence and therefore to define “true-eloquence” and non-eloquent areas. Thus, intraoperative mapping may preserve function and increase the extent of tumor resection at the same time [10, 11]. To guide intraoperative decision-making, when to stop and when to continue resection, various neurophysiological methods are available. Continuous monitoring techniques, for example, monitoring of motor evoked potentials (MEPs), enable real-time assessment of the functional integrity of the observed functional system [12–20]. Electrical cortical mapping is the gold standard for localization of eloquent cortex [21–25]. Subcortical mapping is used to localize white matter tracts at different stages of tumor resection [8, 10, 21, 26–34]. The choice of the intraoperative neurophysiological technique may also depend on the intraoperative pathology, which needs to be treated (Fig. 14.1). Extra-axial lesions such as meningioma differ from infiltrative glioma. Brain plasticity and the goal of supra-marginal resection render intraoperative neurophysiological mapping an essential adjunct in the latter case [30, 35]. However, neurophysiological techniques may reassure the surgeon as well during the resection of cavernoma or metastasis by defining safe entry zones and by influencing the speed of tumor resection [11, 18, 36]. Intraoperative neurophysiological techniques should also be adapted to the tumor location. Tumors close to and in the precentral region may need precise and continuous mapping techniques whereas insular tumors may also need monitoring techniques for vascular ischemia [37–41]. Advances in imaging techniques such as functional MRI and fiber tracking algorithms as well as preoperative navigated transcranial magnetic stimulation examinations may help to plan the surgical approach and to prepare for intraoperative pitfalls. However, after opening the dura and especially after corticotomy and tumor debulking, neuronavigation loses accuracy due to brain shift [42]. Therefore, “maximal safe resection” should be guided by intraoperative neurophysiologic monitoring and mapping methods.

a

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Fig. 14.1 (a) Coronar cut illustrating CST fibres originating from M1 in an healthy brain. (b) An extra-axial tumor such as an meningioma pushes the whole cortex down and may cover and partially infiltrate eloquent areas. Lesions like a cavernoma (c) and a metastasis (d) may displace the CST fibres in an unpredicted trajectory. Glioma infiltrate eloquent tracts (e), and thus, they render resection particulary challegning. (© Inselspital, Bern University Hospital, Dept. of Neurosurgery)

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Monitoring Motor Function Obviously, mapping only provides information at and distal to the stimulation site. If feedback about the whole integrity of the motor or sensory system in an anesthetized patient is needed, monitoring methods for a continuous assessment are recommended [18, 19, 43]. Thus, remote vascular injury due to coagulation of vessel perforators can only be detected by monitoring methods [15–17]. If MEP monitoring under general anesthesia is performed, some requirements for the anesthesia regime should be considered. The standard recommendation is total intravenous anesthesia, but inhalation agents with a low mean alveolar concentration might be possible in selected circumstances. A short-acting relaxant should be administered for intubation purpose only [44, 45]. Recovery from muscle relaxation could be tested by the use of the “train-of-four” technique involving percutaneous stimulation of median nerve applying 40  mA and a 0.2  ms pulse duration [45]. Under general anesthesia, classical short train technique, also called high-­ frequency stimulation, is applied. The temporal summation of multiple descending volleys in high-frequent short train stimulation finally triggers a time-locked MEP response [13, 14]. It typically consists of trains with four-to-nine monophasic rectangular electrical pulses of 200–500 μs pulse width with an inter stimulus interval of 2–4 ms (corresponding to 250–500 Hz) [13, 14, 19, 28, 44, 46]. Continuous MEP monitoring is performed either with via scalp electrodes (transcranial electrical stimulation, TES) or electrodes directly placed on the precentral gyrus (direct cortical stimulation, DCS, Fig.  14.2). For further details on MEP for supratentorial approaches, refer to Chap. 9.

Fig. 14.2 Real-time assessment of direct cortical stimulated MEP via a strip electrode may monitor the functional integrity of M1 and the CST to assess the functional integrity of the primary motor system. Focal cortical stimulation may avoid false-negative results in case of more distal stimulation of the CST to the resection site. MEP will warn for remote vascular injury and help to predict long-term postoperative motor outcome. (© Inselspital, Bern University Hospital, Dept. of Neurosurgery)

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MEP warning criteria represent a priori defined parameters. Optimally, they should alert the surgical team and they prompt the implementation of corrective measures [47]. Obviously, a false-negative reassurance will miss the neurological injury; however, a false-positive alarm may also indirectly harm the patient by stopping the surgery too early [47]. The most common proposed MEP alarm criteria include disappearance of MEP signal, amplitude reduction, and stimulation threshold elevation [48]. Disappearance of MEP signal is considered as a major alarming sign that required reassessment of intraoperative settings and adjustment of surgical strategy. Apart from MEP loss, the most commonly used warning criterion is amplitude reduction, and a >50% amplitude reduction is regarded in the vast majority of studies as significant during supratentorial surgery [16, 46, 49, 50]. Threshold cut-­ off values vary depending on stimulator settings (constant current versus constant voltage stimulation) and electrode montages (TES versus DCS) [51]. Cut-off values that have been used during TES were >100 V or >20 mA and during DCS >3 mA, ≥4 mA, and ≥5 mA. TES may allow bilateral assessment, and therefore, the non-affected side may serve as control for non-surgical factors, like change in anesthetic depth. Therefore, Abboud et al. [52, 53] introduced a novel threshold criterion and suggested that a TES threshold increase on the affected side of more than 20% beyond the percentage increase on the unaffected side should be considered as a warning sign. The stimulation intensity has special importance when interpreting the amplitude criterion, as MEP exhibits trial-to-trial variability and MEP amplitude alterations may be caused by non-surgical factors [48]. Rothwell et al. [54] stated that strong stimulation currents may activate the CST even at the foramen magnum. Hence, depending on the area of interest, there might be the risk of stimulating the white matter more caudally than the site of neurological damage, leading to a higher rate of false-­ negative results. A topographic-guided MEP description is detailed in Chap. 9. Furthermore, loss of cerebrospinal fluid after the opening of the dura leads to brain shift and subdural air accumulation. That fact may interfere with the reliability and evaluation of TES-MEP warning criteria. Further, TES may cause a higher rate of patient movement [18]. Because of these drawbacks, many neurosurgeons opt for DCS, which needs lower stimulation intensities and allows a focal and superficial stimulation of corticospinal neurons [18]. Nonetheless, DCS is not applicable in patients with scar tissue from previous operations. It may also interfere with MEP monitoring due to electrode dislocation on the cortex [50]. Szelényi et al. reported that TES and DCS do not differ in their ability to detect an impending neurological injury. Both paradigms may be alternatively applied during the same surgical procedure, provided if lateral TES montages are not used and near-threshold stimulation intensities are applied [55]. However, a more thorough comparison between the two stimulation modalities depending on the type of surgery, pathology, and tumor location (especially in the precentral area) would be clinically meaningful and may contribute to an optimized implementation of warning criteria [47].

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Monitoring Sensory Function For brain tumor surgery, SEP may be used to detect cortical or subcortical ischemia affecting the somatosensory cortex or lemniscal pathways. A well-established relationship between the critical cortical perfusion of brain parenchyma below 15 ml/100 g/min and a decline of SEP amplitudes is described [56]. Recording of the median and tibial nerve cortical potentials of the unaffected hemisphere may serve as systemic controls to detect factors unrelated to the surgical resection such as the level of anesthesia and body temperature. A 50% amplitude decrement and an increment in the latency of the cortical potential are commonly used as warning criteria. However, smaller amplitude decrements may be significant when trial-to-­ trial reproducibility is high, and disappearance may be needed to detect non-random amplitude reduction when reproducibility is low [57]. A special application is the technique of SEP phase reversal (Fig.  14.3). The phenomenon of recording an inversion of the median nerve cortical SEP polarity between the postcentral and precentral gyri is used to determine the central sulcus [58, 59]. Many surgical teams being very experienced with cortical mapping do not routinely use this methodology as they find that direct cortical mapping provides sufficiently precise information. Nevertheless, SEP phase reversal is an excellent tool considerably helpful in distorted anatomy and inconclusive mapping results [59].

a

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Fig. 14.3  Phase reversal of the ulnar nerve for identification of the central sulcus. (a) Referential technique: grid contacts are individually referred to Fz. (b) Differential technique: bipolar setup of the grid contacts: 1-2, 2-3, 3-4, 4-5, 5-6. Reversal of N20/P22 is seen between 4 and 5 in both techniques

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Subcortical Mapping Distance Estimation Toward CST Identification of mapping alarm criteria for impending mechanical damage of the CST remains a challenge to the surgeon and neurophysiologist. During tumor removal, the surgeon needs to know how distant the resection cavity is at a certain point to the CST. Eliciting an MEP depends on the charge applied to the tissue [28]. The charge density decreases with distance. The higher the charge, the larger the area where MEPs can be generated, and vice versa [18]. This also implies that with higher stimulus intensity or charge a positive stimulation can be found at a greater distance from the CST.  This “stimulation-strength-to-CST-distance” relationship has been increasingly investigated by many groups that have correlated the stimulation intensity in mA needed to elicit MEPs with distance in mm to the CST using different pulse durations [60–65]. One of the first correlations was done by Kamada et al. [60] who found a convergent nonlinear correlation of distance and postulated 1.8 mA as the threshold of direct CST contact during monopolar cathodal subcortical stimulation using trains of five 0.2  ms pulses. Nossek et  al. [62] compared the thresholds of subcortical monopolar mapping using trains of 5–7 0.5 ms pulses at 300 Hz to navigation with brain shift correction by intraoperative ultrasonography. They showed an approximately linear correlation between MEP thresholds and distance to the CST with a relationship of 0.97 mA for every 1 mm of brain tissue, which corresponds to the “rule-of-thumb” of 1 mA = 1 mm [45]. A linear correlation between stimulus intensity and distance was also postulated in another study by Ohue et al. [64] that used trains of five 0.2 ms pulses at 500 Hz and analyzed the distance of the postoperative resection cavity to the imaged CST in early postoperative diffusion tensor imaging MRI. Maesawa et al. [61] and Prabhu et al. [63] compared subcortical stimulation to intraoperative MRI tractography. Maesawa et al. (bipolar probe, train of 5 stimuli, pulse duration 0.4  ms, 500  Hz) found an approximately linear correlation, whereas Prabhu et al. (monopolar probe, train of 5 stimuli, 0.3–0.5 ms, 500 Hz) described a trend toward worsening neurologic deficits if the distance from the probe to the CST was 50% decrease in amplitude or 10% increase in latency after ruling out technical and surgical causes [2]. A transcranial motor evoked potential (MEP) alert can be defined as 80% or more decrement in the amplitude or increase in the stimulation threshold of 100 V or more from the baseline. Successful conduction and interpretation of alterations in IOM has the potential of refining anesthetic care and patient safety. Tewari et al., based on their protocol’s definitions of alerts and notifications during IOM-supported surgeries, observed resolution in 90% of alerts and 80% of notifications when anesthesia team was notified about disturbances in EPs [2].

Patient Selection and Preparation The appropriate patient selection and preparation are fundamental steps for the success of the procedure [3]. For the brain mapping to be successfully performed, the patient must be able to communicate, besides having an adequate degree of understanding and cooperation [4].

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The patient’s educational level and work activity must be known in order to adapt the language and personalize the tests. Pre-anesthetic evaluation should be done electively, with reasonable anticipation, calmly, and seeking to gain the trust of the patient and their family. The degree of anxiety should also be evaluated, since very anxious patients have a high potential to develop agitation on awakening and difficulty in collaborating during the tests. However, the use of pre-anesthetic medications is controversial, as they may impair intraoperative dynamics. Midazolam, for example, can cause respiratory depression, paradoxical psychomotor agitation, and interfere with monitoring [5]. In our routine, we use pre-anesthetic medication as a last resort, and we reinforce that creating an environment of trust is a unique tool in reducing stress. It is essential that the anesthesiologist create a good doctor-patient relationship of trust, as this has a great anxiolytic effect. Describing the surgery step-by-step, besides showing images of previous surgeries, therefore avoiding the “fear of the unknown”, can mitigate the natural anxiety of patients. The anesthesiologist’s role at this moment is, together with the other team members, shape perceptions, manage expectations, and anticipate surprises. However, overly detailed information can have a side effect and lead to increased stress. The key, when detailing to the patient and family a particular conduct that will be adopted, is to link it to the expected benefits and emphasize that several measures taken seek to avoid complications. Also, as important steps in the preoperative period, we should evaluate the airway so that we can anticipate difficult scenarios, as well as notice if any degree of claustrophobia is present. We should look for a history of nausea and vomiting in previous surgeries, convulsions, and intracranial hypertension. Finally, we should be aware of the patient’s comfort level, since the vigil state causes the patient to be exposed to various stressors of several intensities. The operating room needs to be quiet, free of noise, and the professionals involved need to be orderly and control their tone of voice. The positioning of the patient needs to be carefully planned, since he will be awake and practically immobile for several hours. Reducing the fasting time by using carbohydrate-rich preparations also contributes to well-being and a better postoperative prognosis.

Choice of Anesthetic Technique Intraoperative awake craniotomy is a unique clinical scenario where the anesthesiologist must promote analgesia and sedation without interfering with neurophysiologic monitoring and patient cooperation, allowing manipulation of brain tissue, and ensuring adequate ventilation and airway safety. For most brain tumors, resection is not curative. However, the amount of tumor mass resected is related to increased survival, seizure control, and decreased morbidity. Two anesthetic techniques are described and well established for this type of intervention: asleep-awake-asleep and conscious sedation (also called

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awake-­awake-­awake). The goal of both is to allow unconsciousness and analgesia in the craniotomy phase, and rapid return of the patient to consciousness in the awake-­ awake phase for testing. Whichever anesthetic technique is chosen, the main secret to success is the association of the scalp block. The technique known as asleep-awake-asleep involves the use of general anesthesia for the initial preparation and craniotomy. Then, with the brain tissue already exposed, the patient is awakened to perform neurofunctional tests and resection is initiated. At the end of the resection and hemostasis, general anesthesia is induced again, so that the craniotomy can be closed and sutured. Usually a combination of propofol and remifentanil is used due to its pharmacokinetic characteristics that allow rapid awakening. The use of a supraglottic device to control the airway is recommended, so that awakening is smoother and coughing or choking is avoided. It is noteworthy that during fixation of the skull and positioning of the head, it is possible that the supraglottic device may dislodge and leak, requiring repositioning. Therefore, direct communication with the surgical team is necessary to find an adequate position for the surgery and for ventilation not to be impaired. In our routine, we chose the modified asleep-awake-asleep technique, because at the end of the resection and hemostasis we only restart the propofol infusion to achieve mild sedation. This allows the patient to rest after the strenuous testing phase, maintain spontaneous ventilation without us having to reorder the airway. We perform induction with fentanyl, propofol, and lidocaine, and insert a supraglottic device for airway control. Maintenance is done with remifentanil and propofol in a target-controlled infusion. Propofol is the base medication for this regimen, given its easy titration, rapid and gentle awakening, antiemetic properties, and anticonvulsant effect. After anchoring and opening the dura mater, we start the awakening phase by stopping all infusions. We emphasize that the supraglottic device should only be removed during the awakening phase when the patient is responding to commands, so that the risk of respiratory depression is minimal. The choice of general anesthesia with laryngeal mask instead of conscious sedation is due to: (a) the possibility of monitoring and control of ETCO2 before resection; (b) better hemodynamic control; (c) greater comfort for positioning and placement of the fixation pins; (d) greater comfort for scalp block, venous and arterial punctures, for vesical catheterization, and for neurophysiological monitoring. It is worth noting that conscious sedation is necessarily mild and can lead to discomfort, agitation, anxiety, and undesirable hemodynamic changes in neurosurgery. In the case of the conscious sedation technique, sedation is performed from the beginning, keeping the patient on spontaneous ventilation. In the waking phase, the sedation should be diminished so that awakening occurs. In this case, the combination of propofol and remifentanil brings increased risk of respiratory depression, and the use of dexmedetomidine, associated or not with propofol, has become an important tool in this context. However, the optimal degree of sedation is not easy to achieve, and the anesthesiologist needs to be experienced and skilled, because too much sedation can cause respiratory depression or make neurofunctional tests impossible.

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The literature on the use of dexmedetomidine in the context of intraoperative awakening is controversial. The concern about the ability of dexmedetomidine to allow the patient to adequately perform neurofunctional tests has been the subject of several scientific papers. Hall et al. showed that some of the patients in their study were not able to adequately perform the language test with dexmedetomidine infusion of 0.2 and 0.6 μg.kg−1.h−1 [6]. Bekker et al., in their study, reported delay in performing neurofunctional tests due to excessive sedation [4]. Bustillo et  al. reported in their study that performing complex neurofunctional tests was not possible even after 60 min of dexmedetomidine discontinuation [7]. On the other hand, Mack et  al. noted that tests on the patients in their sample were possible [8]. McAuliffe et al. administered a bolus of 1 μg.kg−1 dexmedetomidine in 15 min and 0.3–0.4 μg.kg−1.h−1 in continuous infusion, but discontinued all anesthetics at the onset of dura mater opening [9]. The patients remained without anesthetic infusion during the tests, and the tests were performed successfully. Goettel et al. found no differences in the ability to perform neurophysiologic tests between patients in their sample who received dexmedetomidine and those who received propofol-­ remifentanil [10]. It seems that the best results are achieved when a lower attack dose is used, or even when no attack dose is used, and when the maintenance infusion is stopped well in advance. In our routine, we particularly avoid using dexmedetomidine because of its unpredictable effect, linked to its context-sensitive half-life. The blockade of the nerves that innervate the scalp is fundamental for a pleasant and pain-free awakening. The infiltration of local anesthetic is performed in the trajectory of six specific nerves: supraorbital and supratrochlear, occipital major and minor, auriculo-temporal, zygomatic (Fig.  15.1) [11]. Bupivacaine, levobupivacaine, and ropivacaine promote adequate local anesthesia and are the most frequently used local anesthetics. In our routine, we perform round infiltration of the entire scalp circumference, combined with the infiltration of the sites where the fixation pins were inserted into the scalp. The block is done bilaterally, because better quality of anesthesia brings more comfort to the patient. A solution of levobupivacaine 2.5 mg.ml−1 combined with lidocaine 5 mg.ml−1, dexamethasone 0.1 mg. kg−1, and clonidine 1  g.kg−1 is applied. The anatomical reference of the mastoid process is used to start the infiltration of the anesthetic solution, tracing a line from this point to the occipital prominence. Figures 15.2, 15.3, 15.4, 15.5, 15.6, and 15.7 show how this technique is used in practice.

Anesthesia and IOM Most awake craniotomies are performed under the classic technic “awake-asleep-­ awake,” and a sequence of interventions is executed by the anesthetist before procedure initiation (e.g., monitoring, anesthetic induction, intubation, venous and arterial lines puncture, scalp blockage, and patient positioning). During this

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Fig. 15.1  Topography of the supratrochlear nerve, suprarorbital nerve, major and minor occipital nerves, auriculo-temporal nerve and zygomatic nerve

Auriculotemporal n. Zygomaticotemporal n. Supraorbital n. Suptatrochlear n.

Third Occipital n. Greater Occipital n. Lesser Occipital n.

Fig. 15.2  Major and minor occipital nerve blocks (the author’s personal file)

Fig. 15.3  Scapl block occipital region (greater and lesser occipital nerves) (the author’s personal file)

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Fig. 15.4 Engorgement confirming the deposit of local anesthetic in the proper pathway (the author’s personal file)

Fig. 15.5 Supra-trochlear and supra-orbital nerve blocks (the author’s personal file)

Fig. 15.6 Zygomatic nerve block (the author’s personal file)

sequence, the anesthetist must allow the neurophysiologist to place electrodes. In addition, at the time of positioning, there must be a harmonious organization in order for the various electrophysiological monitoring cables not to get tangled with the anesthesiologist’s monitoring cables, with the venous hydration lines, with the

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Fig. 15.7  Block of the auriculo-temporal nerve (the author’s personal file)

invasive blood pressure monitoring line, or even with the mechanical ventilator tube. Still, we must observe if any of these devices is in contact with the patient’s skin, which can cause pressure damage. Homeostasis is essential during neurosurgery with IOM. Physiologic factors that may influence EPs include temperature, blood pressure, hematocrit, acid-base balance, blood glucose, and oxygen and carbon dioxide tensions. In addition, several drugs can also influence the electrophysiological responses. Thereby, anesthetists are able to support IOM by managing these aspects. It is noteworthy that bolus doses of anesthetics or sudden and pronounced changes in infusion doses impair monitoring because they cause changes in the recording of potentials and compromise the neurophysiologist’s assessment [1].

Pharmacological Effects Anesthesia involves the choice of favorable drug combination and maintenance of a steady state, avoiding changes in concentration or bolus drug delivery during critical monitoring periods [12]. The effect of anesthetics on synaptic transmission is greater than on axonal conduction [13]. For this reason, responses recorded from polysynaptic pathways (e.g., cortical recordings) are affected by anesthesia to a much greater extent than those recorded from oligosynaptic pathways (e.g., spinal cord and subcortical recordings) [14]. This may explain why inhalational agents produce a dramatic nonlinear, dose-dependent reduction in cortical responses, increasing with the number of synapses involved [15]. It is noteworthy that bolus doses of anesthetics or sudden and pronounced changes in their infusion doses impair monitoring, since they cause alteration of the baseline potentials and compromise the neurophysiologist’s evaluation [1].

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Inhalational Agents In general, the inhalational anesthetic agents have the most profound effect on monitoring [16]. All volatile anesthetics produce a dose-dependent increase in SSEP latency, an increase in central conduction time (CCT), and a decrease in amplitude [17, 18]. They may also cause morphologic changes, such as contraction of early cortical waveforms (N-20) into a simple monophasic wave under deep isoflurane [19] or sevoflurane [20] anesthesia. The later cortical waveform components are most sensitive to volatile anesthetics, with marked attenuation at concentrations exceeding 0.5 minimum alveolar concentration (MAC) [19]. How volatile anesthetics differ quantitatively in their effects on the SSEP is not completely settled [1]. Sevoflurane and desflurane are associated with less amplitude reduction than isoflurane at a MAC range of 0.7–1.3 [21]. The newer volatile anesthetics desflurane and sevoflurane affect SSEPs not unlike isoflurane but may permit the use of higher inhaled concentrations [1]. In contrast to their effects on the cortical SSEP, all volatile anesthetics, even at concentrations above 1.0 MAC, only minimally affect the subcortical waveform, resulting in high recordability [21] and reliability. The effect of volatile anesthetics on cortical SSEP amplitude is exacerbated by nitrous oxide [1]. Eliminating nitrous oxide from the background anesthetic has been shown to improve cortical amplitude sufficiently to make IOM more reliable [22]. Potent volatile anesthetics are associated with small increases in BAEP latency but do not affect wave I–V amplitude [23–26]. The prolongation of wave I–V latency and interpeak latency (IPL) reflects the depressant effect of volatile anesthetics on brainstem neuronal activity [26]. In adults, the effect of volatile anesthetics on BAEP latency is dose dependent [27]. In contrast to cortical SSEPs, the action of volatile anesthetics on BAEP latency or amplitude is not affected by 50–70% nitrous oxide [1]. 10–50% nitrous oxide alone also had no effect on the latency, interpeak latency, or amplitude of waves I–V in healthy volunteers [28]. Volatile anesthetic agents produce predictable dose-dependent increases in midlatency auditory evoked potential (MLAEP) latency and decreases in amplitude [26]. At approximately 1 MAC, MLAEP components are markedly attenuated, indicating suppression of cortical auditory processing such as auditory perception, intraoperative wakefulness, and explicit or implicit recall of intraoperative events [29]. In general, all volatile anesthetics markedly prolong VEP latency and decrease amplitude in a dose-dependent manner [30]. The inhalational agents produce minimal changes in the epidurally recorded D-wave of the MEP with dramatic depression of the compound muscle action potential (CMAP) response [31]. The CMAP response of the MEP appears most easily abolished by low concentrations of halogenated inhalational agents [1]. However, MEP monitoring of neurologically normal individuals undergoing spine surgery can frequently be accomplished with the use of 0.5 MAC of desflurane or sevoflurane [31].

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The effects of anesthesia on the EP can be greater in neurologically impaired patients than in patients without preoperative deficits [32]. Several strategies can be used to enhance the amplitude and reproducibility of SSEPs during volatile anesthesia [1]. Technical strategies such as keeping electrode impedance low and using appropriate bandpass filters are important [33]. Increasing the rate of stimulation in patients with normal baseline SSEPs may improve the preservation of SSEP waves, particularly at higher volatile anesthetic concentrations [1]. When IOM is being performed, volatile anesthetics alone at a dose greater than 1 MAC and volatile anesthetics at greater than 0.5 MAC in combination with nitrous oxide should be avoided. Therefore, volatile anesthetics alone at up to 1 MAC can be used, although it is critical to avoid sudden changes in volatile anesthetic depth. However, in general, intravenous anesthetic techniques result in less amplitude and latency perturbation than volatile anesthetics [18].

Intravenous Agents Total venous anesthesia is preferred during IOM because it influences EPs much less than volatile anesthetics. Barbiturates produce a dose-dependent increase in latency and decrease in early cortical SSEP amplitude that does not preclude IOM. Even at much higher doses, such as those used for barbiturate coma, barbiturates allow recording of cortical SSEPs [34]. Barbiturates in doses used for the induction of anesthesia do not affect the BAEP [35]. Amplitude was unchanged in doses used for the induction of anesthesia, and BAEP waveforms were easily recorded even in the presence of an isoelectric electroencephalogram [36]. Etomidate dramatically increases cortical SSEP amplitude (N-20), up to 400% above preinduction baseline in some patients [37], with no changes in subcortical and peripheral sensory responses [38]. Propofol is the most commonly used anesthetic in neurosurgery, especially at the IOM context. Induction produces amplitude depression in cortical SSEPs [16], although SSEP waveforms stabilized within 30 min after anesthetic administration and were compatible with IOM [39]. Propofol suppresses EPs less than other anesthetics, mainly when compared with inhaled agents [1]. The rapid propofol metabolism allows quickly adjustments when EPs are affected. The effects of ketamine on subcortical and peripheral responses are also minimal; it increases the amplitude of the cortical SSEP and MEP CMAP [40]. The use of ketamine with propofol reduces the depressant effect of propofol while providing an enhancement effect on responses. Benzodiazepines have only mild-to-moderate depressant effects on SSEPs [1] and do not change the amplitude or latency of BAEP [41]. Opioids cause only mild depression of all responses [31], but most authors report clinically unimported changes.

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Dexmedetomidine appears to have minimal effects on SSEP responses when combined with opioids [31]. Neuromuscular blocking agents do not directly influence SSEP, BAEP, or VEP [42]. However, depression of the neuromuscular junction impairs MEP and electromyography (EMG) monitoring [31].

Complications The most common complications are seizure, airway emergence, hypertension, desaturation, nausea and vomiting, cerebral edema, insufficient duration of scalp block, and inability to perform neurofunctional tests. Failure due to the patient’s inability to perform neurofunctional tests is commonly caused by seizure, cerebral edema, dysphasia, and somnolence [43]. Convulsion is an infrequent event. If it occurs, any electrical stimulation should be discontinued, and the surgeon should promptly irrigate the brain tissue with ice-­ cold saline solution. If it persists, a small dose of propofol is recommended. We should avoid benzodiazepines, as the prolonged effect may make it impossible to continue neurofunctional testing. Fortunately, airway instrumentation is usually not necessary [44]. Emergency airway supplies should always be available. If ventilatory depression occurs, generally placing a Guedel tube and performing manual ventilation with a face mask is successful. In any case, a laryngeal mask should be available if the need arises. Cerebral edema should be treated by elevating the head, improving ventilation with a consequent reduction in the CO2 level, and controlling blood pressure. The use of hyperosmolar solutions such as mannitol or hypertonic saline may be required. In some situations, these measures may be ineffective, and tumor surgical emptying may be necessary to improve the operative site. Arterial hypertension is not desirable as it compromises resection. However, vasodilators cause cerebral vasodilation and should be used with caution. In this situation, if there is no contraindication, beta-blockers can be used. Failure to perform neurofunctional tests requiring conversion to general anesthesia is rare. A meta-analysis showed that both the asleep-awake-asleep technique and the conscious sedation technique are similar in relation to the occurrence of major adverse events [5].

Conclusion Intraoperative awake craniotomy reduces the length of stay in the hospital, potentially reducing the risk of infection and thromboembolic events, and shortens the interval between surgery and chemotherapy [45].

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Accumulating evidence suggests that, compared with surgery under general anesthesia, craniotomy with intraoperative awakening is associated with better outcomes, including greater extent of tumor resection, less subsequent neurological deficit, shorter hospital stay, and increased survival [45]. In this scenario, the decisions made by the anesthesiologist have great influence on the intraoperative success and postoperative clinical outcome. The anesthesiologist should, to minimize the impact on evoked potentials, preserve adequate homeostasis, use intravenous anesthetics whenever possible, avoid bolus doses or sudden and large changes in infusions, and notify the neurophysiologist whenever any change or modification in the anesthetic regimen occurs.

References 1. Banoub M, Tetzlaff JE, Schubert A. Pharmacologic and physiologic influences affecting sensory evoked potentials: implications for perioperative monitoring. Anesthesiology [Internet]. 2003;99(3):716–37. Available from: https://doi.org/10.1097/00000542-­200309000-­00029. 2. Tewari A, Francis L, Samy RN, Kurth DC, Castle J, Frye T, et al. Intraoperative neurophysiological monitoring team’s communiqué with anesthesia professionals. J Anaesthesiol Clin Pharmacol. 2018;34(1):84–93. 3. Alcaraz García-Tejedor G, Echániz G, Strantzas S, Jalloh I, Rutka J, Drake J, et al. Feasibility of awake craniotomy in the pediatric population. Paediatr Anaesth. 2020;30(4):480–9. 4. Bilotta F, Rosa G. “Anesthesia” for awake neurosurgery. Curr Opin Anaesthesiol. 2009;22(5):560–5. 5. Sewell D, Smith M. Awake craniotomy: anesthetic considerations based on outcome evidence. Curr Opin Anaesthesiol. 2019;32(5):546–52. 6. Hall JE, Uhrich TD, Barney JA, Arain SR, Ebert TJ. Sedative, amnestic, and analgesic properties of small-dose dexmedetomidine infusions. Anesth Analg. 2000;90(3):699–705. 7. Bustillo MA, Lazar RM, Finck AD, Fitzsimmons B, Berman MF, Pile-Spellman J, et  al. Dexmedetomidine may impair cognitive testing during endovascular embolization of cerebral arteriovenous malformations: a retrospective case report series. J Neurosurg Anesthesiol. 2002;14(3):209–12. 8. Mack PF, Perrine K, Kobylarz E, Schwartz TH, Lien CA. Dexmedetomidine and neurocognitive testing in awake craniotomy. J Neurosurg Anesthesiol. 2004;16(1):20–5. 9. McAuliffe N, Nicholson S, Rigamonti A, Hare GMT, Cusimano M, Garavaglia M, et  al. Awake craniotomy using dexmedetomidine and scalp blocks: a retrospective cohort study. Can J Anaesth. 2018;65(10):1129–37. 10. Goettel N, Bharadwaj S, Venkatraghavan L, Mehta J, Bernstein M, Manninen PH. Dexmedetomidine vs propofol-remifentanil conscious sedation for awake craniotomy: a prospective randomized controlled trial. Br J Anaesth. 2016;116(6):811–21. 11. Guilfoyle MR, Helmy A, Duane D, Hutchinson PJA. Regional scalp block for postcraniotomy analgesia: a systematic review and meta-analysis. Anesth Analg. 2013;116(5):1093–102. 12. Sloan TB. General anesthesia for monitoring. In: Monitoring the nervous system for anesthesiologists and other health care professionals. New York: Springer; 2012. p. 319–35. 13. Richards CD.  Actions of general anaesthetics on synaptic transmission in the CNS.  Br J Anaesth. 1983;55(3):201–7. 14. Samra SK, Vanderzant CW, Domer PA, Sackellares JC.  Differential effects of isoflu rane on human median nerve somatosensory evoked potentials. J Am Soc Anesthesiol. 1987;66(1):29–35.

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15. Sloan TB, Heyer EJ. Anesthesia for intraoperative neurophysiologic monitoring of the spinal cord. J Clin Neurophysiol. 2002;19(5):430–43. 16. Sloan T, Jameson L, Janik D, Koht A.  Evoked potentials. In: Cottrell J, Patel P, editors. Neuroanesthesia. 6th ed. Elsevier; 2017. p. 114–26. 17. Pathak KS, Amaddio MD, Scoles PV, Shaffer JW, Mackay W.  Effects of halothane, enflurane, and isoflurane in nitrous oxide on multilevel somatosensory evoked potentials. J Am Soc Anesthesiol. 1989;70(2):207–12. 18. Sebel PS, Ingram DA, Flynn PJ, Rutherfoord CF, Rogers H. Evoked potentials during isoflurane anaesthesia. BJA: Br J Anaesth. 1986;58(6):580–5. 19. Porkkala T, Kaukinen S, Häkkinen V, Jäntti V. Median nerve somatosensory evoked potentials during isoflurane anaesthesia. Can J Anaesth. 1997;44(9):963–8. 20. Rytky S, Huotari AM, Alahuhta S, Remes R, Suominen K, Jäntti V. Tibial nerve somatosensory evoked potentials during EEG suppression in sevoflurane anaesthesia. Clin Neurophysiol. 1999;110(9):1655–8. 21. Rehberg B, Rüschner R, Fischer M, Ebeling BJ, Hoeft A.  Concentration-dependent changes in the latency and amplitude of somatosensory-evoked potentials by desflurane, isoflurane and sevoflurane. Anasthesiol Intensivmed Notfallmedizin Schmerztherapie AINS. 1998;33(7):425–9. 22. Porkkala T, Janit V, Kaukinen S, Hakkinen V.  Nitrous oxide has different effects on the EEG and somatosensory evoked potentials during isoflurane anaesthesia in patients. Acta Anaesthesiol Scand. 1997;41(4):497–501. 23. Manninen PH, Lam AM, Nicholas JF. The effects of isoflurane and isoflurane-nitrous oxide anesthesia on brainstem auditory evoked potentials in humans. Anesth Analg. 1985;64(1):43–7. 24. Madler C, Keller I, Schwender D, Pöppel E.  Sensory information processing during general anaesthesia: effect of isoflurane on auditory evoked neuronal oscillations. Br J Anaesth. 1991;66(1):81–7. 25. Schwender D, Klasing S, Conzen P, Finsterer U, Pöppel E, Peter K.  Midlatency auditory evoked potentials during anaesthesia with increasing endexpiratory concentrations of desflurane. Acta Anaesthesiol Scand. 1996;40(2):171–6. 26. Schwender D, Conzen P, Klasing S, Finsterer U, Poppel E, Peter K. The effects of anesthesia with increasing end-expiratory concentrations of sevoflurane on midlatency auditory evoked potentials. Anesth Analg. 1995;81(4):817–22. 27. Thornton C, Heneghan CPH, James MFM, Jones JG. Effects of halothane or enflurane with controlled ventilation on auditory evoked potentials. Br J Anaesth. 1984;56(4):315–23. 28. Sebel PS, Flynn PJ, Ingram DA. Effect of nitrous oxide on visual, auditory and somatosensory evoked potentials. Br J Anaesth. 1984;56(12):1403–7. 29. Schwender D, Klasing S, Madler C, Pöppel E, Peter K. Midlatency auditory evoked potentials and cognitive function during general anesthesia. Int Anesthesiol Clin. 1993;31(4):89–106. 30. Chi OZ, Field C. Effects of isoflurane on visual evoked potentials in humans. Anesthesiology. 1986;65(3):328–30. 31. Edmonds HL Jr. Multi-modality neurophysiologic monitoring for cardiac surgery. Heart Surg Forum. 2002:225–8. 32. Gillerman R, Duncan J, Bolton J. Prolonged somatosensory evoked potential depression following a brief exposure to low concentrations of inhalation anaesthetic in a 3-year-old child. Pediatr Anesth. 2000;10(3):336–8. 33. Kalkman CJ, ten Brink SA, Been HD, Bovill JG. Variability of somatosensory cortical evoked potentials during spinal surgery. Effects of anesthetic technique and high-pass digital filtering. Spine (Phila Pa 1976). 1991;16(8):924–9. 34. Sutton LN, Frewen T, Marsh R, Jaggi J, Bruce DA. The effects of deep barbiturate coma on multimodality evoked potentials. J Neurosurg. 1982;57(2):178–85. 35. Duncan PG, Sanders RA, McCullough DW.  Preservation of auditory-evoked brainstem responses in anaesthetized children. Can Anaesth Soc J. 1979;26(6):492–5.

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36. Drummond JC, Todd MM, U HS. The effect of high dose sodium thiopental on brain stem auditory and median nerve somatosensory evoked responses in humans. J Am Soc Anesthesiol. 1985;63(3):249–54. 37. McPherson RW, Sell B, Traystman RJ. Effects of thiopental, fentanyl, and etomidate on upper extremity somatosensory evoked potentials in humans. J Am Soc Anesthesiol. The American Society of Anesthesiologists. 1986;65:584–9. 38. Koht A, Schütz W, Schmidt G, Schramm J, Watanabe E.  Effects of etomidate, midazolam, and thiopental on median nerve somatosensory evoked potentials and the additive effects of fentanyl and nitrous oxide. Anesth Analg. 1988;67(5):435–41. 39. Borrissov B, Langeron O, Lille F, Gomola A, Saillant G, Riou B, et  al. Combination of propofol-­sufentanil on somatosensory evoked potentials in surgery of the spine. Ann Fr Anesth Reanim. 1995;14:326–30. 40. Schubert A, Licina MG, Lineberry PJ. The effect of ketamine on human somatosensory evoked potentials and its modification by nitrous oxide. J Am Soc Anesthesiol. 1990;72(1):33–9. 41. Schwender D, Klasing S, Madler C, Pöppel E, Peter K. Effects of benzodiazepines on mid-­ latency auditory evoked potentials. Can J Anaesth. 1993;40(12):1148–54. 42. Sloan TB. Nondepolarizing neuromuscular blockade does not alter sensory evoked potentials. J Clin Monit. 1994;10(1):4–10. 43. Nossek E, Matot I, Shahar T, Barzilai O, Rapoport Y, Gonen T, et al. Failed awake craniotomy: a retrospective analysis in 424 patients undergoing craniotomy for brain tumor. Clinical article. J Neurosurg. 2013;118(2):243–9. 44. Meng L, McDonagh DL, Berger MS, Gelb AW. Anesthésie pour craniotomie éveillé: guide pratique pour le praticien occasionnel. Can J Anesth. 2017;64(5):517–29. 45. Blanshard HJ, Chung F, Manninen PH, Taylor MD, Bernstein M. Awake craniotomy for removal of intracranial tumor: considerations for early discharge. Anesth Analg. 2001;92(1):89–94.

Chapter 16

Anatomy: Language Network and DTI João Tiago Alves-Belo

Abbreviations AF DTI FAT HDFT IFOF ILF ITG LLG MdLF MTG pre-SMA SLF SMA STG UF

Arcuate fasciculus Diffusion tensor imaging Frontal aslant tract High-definition fiber tracking Inferior fronto-occipital fasciculus Inferior longitudinal fasciculus Inferior temporal gyri Low-grade gliomas Middle longitudinal fasciculus Middle temporal gyri Pre-supplementary motor area Superior longitudinal fasciculus Supplementary motor area Superior temporal gyri Uncinate fasciculus

Introduction The human language faculty is a cognitive capacity shared by all normal humans but no other species on the planet [1]. Several definitions can be attributed to it, but it is essentially the capacity of human beings to express themselves, allowing us to

J. T. Alves-Belo (*) Neurosurgery Department, Hospital Felício Rocho, Belo Horizonte, MG, Brazil © The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 S. M. Verst et al. (eds.), Intraoperative Monitoring, https://doi.org/10.1007/978-3-030-95730-8_16

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live in community. Spoken language is an exceedingly complex faculty that allows us to encode, elaborate, and communicate thoughts and experiences by mediating arbitrary symbols known as words [2]. Preserving language is a challenge when we face diseases that involve eloquent brain areas. Several conditions can impair communication, and its treatment may be associated with the risk of permanent deficits, which severely reduces the quality of life of the patients. Low-grade gliomas (LGG), for instance, are typically located within eloquent areas and can involve brain regions related to language in about 50% of the cases [3]. For those who intend to deal with brain lesions related to language, understanding the anatomy and functional basis of the language network is paramount. This chapter aims to review the current language model under an anatomical and functional view based on traditional fiber dissections made as proposed by Klingler [4] and also with the aid of high-definition fiber tracking (HDFT) based on the use of diffusion tensor imaging (DTI) [5].

The Classic Language Model, History, and Evolution Understanding how the brain can create effective communication has been a challenge for researchers over the centuries. Pierre Broca and Carl Wernicke have a vital contribution in this field. Their work has been applied for several years. Broca did his research through observations of patients who had different lesions affecting the left inferior frontal gyrus. He observed that these patients lost their ability to articulate words, while their “memory of the words” and “action of the nerves and muscles of phonation and articulation” were preserved [6]. Few years after Broca’s theory was spread, Wernicke observed that lesions in the posterior superior temporal lobe caused paraphasic errors with impaired naming, repetition, and comprehension. However, the fluency of speech was preserved [7]. He named this region “the area of word images” and further postulated that this region was connected to the inferior frontal region described by Broca. Therefore, Wernicke proposes that the language function was distributed in the two different cortical sites: an anterior frontal cortex involved in motor processing and a posterior temporal cortex performing sensory functions [8]. The arcuate fasciculus would make the connections between these two areas. Wernicke believed that lesions involving this bundle of fibers result in the so-called conduction aphasia, which was subsequently confirmed by Lichtheim in the clinic scenario [9]. In the subsequent decades, this approach to brain function raised a wave of criticisms, and the clinic-anatomical correlation method came under attack by many prominent investigators [2, 8]. On the other hand, the localizationist theories gained strength after the work of Brodmann and Penfield. Brodmann mapped the human cortex in 52 distinct cortical areas based on cytoarchitectonic features. He then postulated that regions with different histologic structures performed different functions [10]. Based on direct electrical stimulation (DES), Penfield, in his turn,

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mapped the somatosensory and motor cortices of the human brain. He also attributed different manifestations to stimulations of temporal and parietal lobes [11]. The idea that each brain function is rigidly localized in a particular cortical area of the brain and an injury to a specific area of the cortex would lead to a loss of corresponding brain function became prominent. In this view, cortices or cortical areas where neurons are located are more relevant when considering the functional aspects of the brain rather than white matter [12]. This dialectic between the localizationists and their opponents lasted for several decades until the work of Geschwind, in the 1960s, pacified the question through new insights into the functional role of connections and specialized cortical areas [2]. He proposed that disconnections syndromes could be induced by lesions involving the white matter and the association cortex. For language, he argued that the perisylvian cortex acts as a relay station between Wernicke’s and Broca’s areas. Therefore, conduction aphasia would be generated to either a lesion in the arcuate fasciculus or the association perisylvian cortex, notedly the angular gyrus [13]. These ideas were compiled as the Wernicke-Geschwind language model (Fig. 16.1). In this theory, a sensory word image would be formatted when an individual first heard a word; given the cortico-cortical connections between the two primary language areas, it would precipitate the simultaneous formation of a motor word image [8]. Although these motor and sensitive words were formatted from the same stimulus, they are not equivalent concepts. The sensory word is located at the auditory cortex, and the meaning attributed to it is diffusely spread through connections coming from the two language centers. Therefore, the spontaneous speech production demands “awakening” of the concept (diffusely located) that activates the sensory

Fig. 16.1  Classical model of language organization proposed based on the Wernicke and Geschwind theory. Broca’s area (represented in blue), located in the inferior frontal gyrus, is the motor center of language, and Wernicke’s area (represented in green), located in the posterior temporal region, is the sensitive word center. The connection of these two language centers is made through the arcuate fasciculus. Cortico-cortical connections coming from these two areas (blue and green arrows) would be responsible for linking the primary language center and the perisylvian cortex, where the language concepts are located

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word yet created (Wernicke’s area) and precipitates the selection of the corresponding motor word (Broca’s area) [8, 13]. Although the new insights coming from the Geschwind have increased the scope and solved some inconsistencies that were present since the Broca and Wernicke ideas, this classical model still had some inconsistencies that raised doubts. The Wernicke-Geschwind model predicts lesions involving the arcuate fasciculus would generate the same deficit, independent of its segment affected, which is not clinically observed [2]. This model was revealed to be an oversimplification since it could not recognize the complexity of linguistic processing that we now know involve different language domains such as lexical, phonological, and semantic [8, 14]. Even the fundaments of the classical model were in check after the advances in neuroimaging. It is known that Broca’s area lesions do not cause the so-called Broca’s aphasia; instead, it demands lesions in broader areas such as the precentral gyrus. Lesions limited to the original Broca’s area generate a transient deficit or a milder aphasia [8, 12, 15]. In a recent paper, Dronkers et al. submitted the brains used by Broca to fundament his theory to MRI, which revealed that their lesions were not confined to the left inferior frontal gyrus but involved deeper structures such as the superior longitudinal fasciculus [16]. Recent advances in neuroscience have demonstrated that the brain is organized as complex, multimodal, and integrated parallel distributed networks, with cognitive processes consisting of a continuous and often redundant stream of information dynamically modulated by experience and the external environment [12, 17]. Catani introduced the concept of “hodotopy,” which gives importance to the cortical epicenters and assumes the relevance of the connectivity of different areas [17, 18]. Under the light of these new neuroscience concepts, the classical language model has been replaced by a new contemporary model.

The Contemporary Language Model When considering the neural basis of a function or dysfunction, mainly cognitive functions such as language, it is essential to focus not only on cortices but also on both cortices and white matter as a network [12]. Language execution is a higher cognitive function that demands several processes, requiring executive resources and involvement of a range of brain areas. Language comprehension, for example, involves auditory and visual word recognition, lexical and morphological processes, syntactic analysis, conceptual interpretation, and referential processes [7]. In this scenario, the current language model is organized in a dual-stream framework. This model was proposed by Hickok and Poeppel [14, 19, 20] and used similar concepts as used for auditory [21] and visual processes [22] already accepted in modern neuroscience. It is essential to mention that Wernicke initially conceived these general concepts. He was the first who proposed, in 1874, that sensory representations of speech in the left posterior temporal lobe interact with two different systems, a broadly diffused conceptual system for comprehension and the motor

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system to engage in speech production. Therefore, the recent model’s major contribution has been the refinement of anatomical localization, specification of language subprocesses, and confirmation, which demanded the best available evidence provided by modern imaging methods and careful lesion-deficit studies [8]. The Hickok-Poeppel model argues that language processing begins with a spectrotemporal analysis supported by the auditory cortices in both hemispheres. Thus, computed information moves to the phonological network in the middle to a posterior portion of the cortex in and around the superior temporal sulcus; information then moves via the dorsal stream, which is strongly left-lateralized and supports auditory-motor integration in speech processing. At the same time, this information travels through the ventral stream, which is bilateral, with a slight left hemisphere bias, and supports auditory comprehension. The dorsal stream’s posterior part involves a segment of the Sylvian fissure at the parietotemporal boundary, supporting the auditory-motor interface. Its anterior portion, in the frontal lobe, includes Broca’s area and its surrounding, which, together with its more dorsal premotor component, supports processes relating sound to speech. The ventral stream’s posterior portion (posterior middle and inferior portions of the temporal lobes) supports the linking of phonological and semantic information (the lexical interface). In contrast, its more anterior areas support combinatorial semantic processes [7, 19] (Fig. 16.2). Therefore, this contemporary model assumes that the semantic processing, performed by the ventral stream, is bilaterally located, with a slight left dominance. The speech perception tasks, executed by the dorsal stream, are strongly

Fig. 16.2  Contemporary dual-stream language model as proposed by Hickok and Poeppel. The language processing begins with a spectrotemporal analysis supported by the auditory cortex (red region); information moves to the phonological network in the middle to a posterior portion of the cortex in and around the superior temporal sulcus (orange region). The information then moves via the dorsal stream (dark blue lines), which supports auditory-motor integration in speech processing, to achieve the premotor cortex (pink region), inferior frontal gyrus (blue region), and parietotemporal boundary region (green region). This information is also carried by the ventral stream (dark red line), which supports auditory comprehension, to achieve the anterior and middle temporal lobe (dark blue region). In this dual-stream model, the dorsal stream is left-lateralized, and the ventral stream is bilateral with a slight left predominance

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left-­dominant. Unilateral temporal damages will not cause speech recognition deficits, whereas speech production deficits are prominent sequelae of dorsal temporal and frontal lesions in the left hemisphere [19]. Duffau has an extensive work based on DES during awake surgery demonstrating the segmentation of the language subprocess that supports the dual-stream model [23]. DES has demonstrated that the dorsal stream has a phonological function in speech production and is mainly composed of the arcuate fasciculus. In contrast, the main tract of the ventral stream is the inferior fronto-occipital fasciculus, which has a semantic function in language processing [23, 24]. The anatomical description of the main tracts which form the dorsal and ventral streams will be made in the subsequent sections of this text.

 iber Tracks’ Morphology, from Klingler F to DTI Tractography The adoption of the new hodotopic framework gave similar importance to the white matter and cortex. In this way, comprehension of the language network demanded a better understanding of the fiber tracts implicated in language, as this knowledge had been neglected for decades. Klinger described a technique for fiber dissection based on fixation of the specimen in 5% formalin followed by freezing the brains before dissection [25]. His technique was diffusely spread by anatomists and made possible a systematization of the fiber dissections. The classical Klinger’s technique was used for Türe in brilliant papers that brought attention for neurosurgeons to the necessity of understanding the white matter tracts [26, 27]. Although the fiber dissection provides a better understanding of the fiber tracts, it is limited for anatomical purposes since it does not allow in  vivo studies. Nowadays, modern neuroradiological studies have allowed a detailed study of the human white matter, especially after the advent of tractography based on diffusion tensor imaging (DTI) [28]. This imaging method utilizes the principles of water molecules’ diffusibility to track fiber bundles in the encephalon. Free water molecules move randomly following the principle of the Brownian movement. Therefore, water molecules do not have a directional preference, which is called an isotropic movement. On the other hand, when the water molecules are inside a fiber tract, it will move in the fiber axis, thus having an anisotropic movement (Fig. 16.3). DTI fiber tracking technique analyzes the diffusion of water molecules in the brain tissue. The direction of the highest diffusivity coincides with the white matter fiber tract axis. Variation of the diffusion along different spatial directions provides information about diffusion anisotropy and, ultimately, tissue architecture [29]. Currently, DTI fiber tracking has been widely utilized in both anatomy studies and surgical planning in neurosurgery [5, 30–33]. In the next section of this chapter,

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Fig. 16.3  The isotropic movement of free water molecules respects the Brownian movement, where the particles move randomly with no directional preference (left side). When inside a bundle, the water molecules tend to move preferentially in the fiber axis, called an anisotropic movement (right side)

the anatomy of fiber tracks related to language will be discussed. The Klingler technique and DTI fiber tracking were used to delineate the complex architecture of the language network. DTI fiber tracking was made using the DSI studio software (http://dsi-­studio.labsolver.org). The three-dimensional reconstruction of fiber tracts on DSI studio followed the general color map, so the green color indicates that a given bundle has an anterior to posterior direction. A fiber orientated in a latero-­ lateral direction will be represented in red color. The blue color will be used to represent tracts that have superior to inferior direction. Fibers that have oblique direction will be represented in a mix of these three colors proportionally.

The Anatomy of the Language Network The human language is a higher cognitive function that requires several processes working together, demanding organizational resources, and involving a range of brain areas. The white mater acts providing the complex network of different brain areas that work in conjunction to execute the speech. A given cortical region can have four main types of connectivity patterns: (1) locoregional connectivity, mediated through short association or U-fibers; (2) subcortical connectivity, which connects different regions of both hemispheres through the long association bundles (horizontal connectivity); (3) interhemispheric connectivity, made by commissural fibers; and (4) the vertical connectivity, mediated by projection fibers and allowing the modulation of cortical processing by deep gray nuclei [17]. The U-fibers are tiny association fibers that connect different gyri in the same hemisphere; they are the most superficial white matter fibers in the human brain and are also called intergyral fibers (Fig. 16.4). As a general principle, deeper tracts used to be longer than superficial ones [34].

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Fig. 16.4  The short association or U-fibers are the most superficial white matter fibers. Located immediately deeper to the cortex, they connect neighboring gyri. (a) The cortex of the frontal and temporal lobes has been removed, exposing the U-fibers of these regions. (b) Closer view of the U-fibers. The dotted lines represent the trajectory of these fibers

The major tracts of the dorsal stream are the arcuate fasciculus (AF), a frontotemporal connection bundle, and the superior longitudinal fasciculus (SLF), which consists of frontoparietal connection fibers.

Superior Longitudinal Fasciculus The SLF defines a set of frontoparietal connections which are classically segmented in three separate subcomponents based on a monkey brain study: the most dorsal component of the SLF is the SLF-I, the second branch is SLF-II, and the most ventral branch is SLF-III [35]. These findings were adopted for the human brain after some papers confirming these segmentations [36, 37]. In this way, the SLF-I is located deeply in the superior frontal gyrus. The SLF-II is located more profound in the middle frontal gyrus, and the SLF-III, the shorter and most superficial segment, lies in the deep of the inferior frontal gyrus [34] (Fig. 16.5). The SLF-III is the shortest segment of the SLF. It is located within the frontoparietal operculum and connects the pars opercularis of the inferior frontal gyrus and the ventral precentral gyrus to the supramarginal gyrus in the inferior parietal lobule. After removing the short association fibers in the middle frontal gyrus, the SLF-II can be found. This segment is located immediately deeper to the SLF-III and is also longer. It courses between the angular and middle frontal gyri at the level of the upper edge of the atrium and the body of the lateral ventricle [34]. The SLF-I is believed to be a connection of the superior frontal gyrus and precuneus region. There are some controversies in the characterization of this tract. Some authors were not able to distinguish these fibers in brain dissections or DTI tractography [26, 38, 39]. As the SLF-I is located deeper to the SLF-II and medial to the corona radiata in a supracingulate region, this bundle should be understood as a segment of the cingulum, reserving the term superior longitudinal fasciculus to the more lateral tracts. In this view, SLF-II would be named as “dorsal SLF,” and

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Fig. 16.5  The superior longitudinal fasciculus is a set of fibers connecting the frontal and parietal lobes. It is generally segmented in three different bundles. (a) Illustration demonstrating the general arrangement of the SLF segments. The SLF-I is the more profound and more prolonged segment; it is located within the superior frontal gyrus and connects the medial and dorsal parietal cortex and precuneus (BA 5 and 7) to the dorsal and medial part of the frontal lobe (BA 8, BA 9, and BA 32). The SLF-II runs deep in the middle frontal gyrus connecting the inferior parietal region (BA 39) and the posterior regions of the superior and middle frontal gyrus (BA 6, BA 8, and BA 9). The SLF-III, located in the inferior frontal gyrus, connects the inferior parietal lobule to the inferior frontal gyrus (BA 44, 45, 47). (b) Fiber dissection of a left hemisphere. The U-fibers of the perisylvian region have been removed, exposing the long association fibers. The SLF-III is the more superficial segment of the SLF situated just lateral to the arcuate fasciculus (AF), located just lateral to the SLF-II, also superiorly situated concerning the AF. (c) Closer view of the perisylvian region tracts demonstrating the intimal relations and the relative position between the AF, SLF-II, and SLF-III. (d) DTI fiber tracking reconstruction of the SLF components. The SLF-I is located in the superior frontal gyrus connecting the medial portion of the superior parietal lobule and the medial portion of the superior frontal gyrus. The SLF-II is located laterally to the SLF-I, in the interior of the middle frontal gyrus, linking the middle frontal gyrus to the inferior parietal lobule. The SLF-III is the shorter and most superficial segment of the SFL, situated within the inferior frontal gyrus. It connects the posterior portion of the inferior frontal gyrus to the inferior parietal lobule. (e) Superior view of the left hemisphere. The SLF-II and SLF-III are exposed as well as the temporal terminations of the AF. The SLF-II is situated superior and medial to the SLF-III and AF. The frontal aslant tract can be seen. It is located medial and crosses the SLF-II inferiorly. The AF turns around the insula to reach the posterior temporal region; the SLF components parallel the superior imitating sulcus of the insula, terminating at the inferior parietal lobule. (f) Fiber tract reconstruction of the SLF-II (represented in yellow color), the SLF-III (represented in red color), and the AF (green color) in the lateral surface of the left hemisphere. The AF lies in between the SLF-III, situated laterally, and the SLF-II superior and medially situated

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Fig. 16.5 (continued)

SLF-­III can be named as “ventral SLF” as proposed by the Fernandez-Miranda group [39]. The SLF-III has a clear role in language, as a component of the dorsal stream. It is involved in decoding visual information to articulation through visuo-­phonological conversion in the phonological processing (working memory) [8, 23, 24, 34]. This bundle’s DES will elucidate speech arrest, phonemic paraphasia, and articulatory disorders [8, 40]. The SLF-II is also implicated in language, but its role is still unclear. Nevertheless, there are several differences in the architecture of this tract when we compare the left and right sides [39]. In a clinical scenario, DES of the SLF-II generates speech arrest and dysarthria. The current data do not implicate SLF-I on language production.

Arcuate Fasciculus The AF comprises a set of fibers that connects the inferior frontal gyrus and the posterior temporal regions. Reil was the first to identify a group of fibers in the perisylvian region that connects frontal, inferior parietal, and posterior temporal regions. Burdach, in 1922, detailed this tract and named it fasciculus arcuatus [2]. Since then, several descriptions of this tract have been made. Some authors consider it a segment of the superior longitudinal fasciculus [24, 32, 38]. However, modern descriptions based on DTI and fiber dissection have demonstrated that the AF is a distinct tract [34, 39]. Utilizing high-definition fiber tracking and careful dissection is possible to separate these tracts. Also, based on anatomical principles, the SLF is a tract that connects frontal and parietal lobes; on the other hand, the AF should be understood as a tract that links frontal and temporal lobes [26] (Fig. 16.6). The AF has a significant dominance in the left hemisphere [37, 41]. There are four different cortical termination of the AF fibers in the frontal region: pars opercularis, pars triangularis, precentral gyrus (ventral portion), and middle frontal gyrus (caudal portion) [41]. In the temporal lobe, the fibers of AF connect to the superior (STG), middle (MTG), and inferior (ITG) temporal gyri. Classically, this

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Fig. 16.6  The arcuate fasciculus is a bundle of fibers that connects the inferior frontal region to the posterior portion of the temporal lobe. (a) The frontal terminations of the AF include the pars triangularis (BA 45), the pars opercularis (BA 44), the ventral precentral and caudal middle frontal gyri (BA6), and the dorsolateral prefrontal cortex (BA 9). In the temporal lobe, the AF terminates in the middle and posterior portion of the superior temporal gyrus (BA 22 and BA 42), rostral middle temporal gyrus (BA 21), and caudal middle temporal gyrus and inferior temporal gyrus (BA 37). (b) Fiber dissection of the left hemisphere demonstrating the AF terminations. The AF begins in the inferior frontal region, turns around the insula, and terminates at the posterior temporal region, reaching the superior, middle, and inferior temporal gyri. The SLF-III lies in the inferior frontal gyrus and is located lateral to the AF. The SLF-II is situated medial and superior to the AF. (c) Closer view of the AF. The SLF segments and insular cortex have been removed. The AF has a C-shaped format connecting the inferior frontal and posterior temporal regions. (d) DTI reconstruction of the left AF in the directional color map demonstrating its general aspect on MRI fiber tract reconstruction. (e) Perisylvian fiber tracts. The SLF-II and SLF-III connect the frontal and inferior parietal regions. The AF turns around the insula connecting the inferior frontal and posterior temporal regions; its temporal terminations are located lateral to the middle longitudinal fasciculus, connecting the superior temporal gyrus with the superior parietal lobule. (f) Three-­ dimensional reconstruction of the subcomponents of the AF. The ventral AF (green) interconnects STG and rostral MTG with the pars opercularis and most ventral premotor cortex. The dorsal AF (red) links ITG and caudal MTG with the ventral precentral and caudal middle frontal gyrus

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tract is described as having a direct segment that links the inferior frontal and posterior temporal regions, connecting the primary language areas, and an anterior indirect segment that connects frontal and parietal regions as well as a posterior indirect segment that connects the inferior parietal and posterior temporal regions [2, 42]. More recent studies suggest a different segmentation of the AF. Based on DTI-­ based tractography and fiber dissections, it was observed that the subset of fibers that comes from the ITG and caudal MTG terminates on the ventral precentral and caudal middle frontal gyrus comprising a dorsal or outer segment of the AF. In its turn, the inner or ventral AF interconnects STG and rostral MTG with pars opercularis and most ventral premotor cortex [41, 43]. In this conception, the anterior and posterior indirect segments described by Catani would be part of the SLF-III and temporoparietal aslant tract, respectively [44]. Functionally, the ventral AF connects the primary language areas being associated with phonological language processing. The dorsal segment interconnects the supplementary language areas associated with lexical and semantic language processing [41, 43]. Stimulation of the AF during awake craniotomies leads to phonemic paraphasias, anomia, and phonological errors [24, 45, 46]. Syntactical errors have also been attributed to the AF based on DTI tractography and subcortical stimulation studies [47, 48].

Frontal Aslant Tract Recent studies have confirmed the presence of connections between the inferior frontal and medial superior frontal gyrus [49]. Although the term frontal aslant tract (FAT) was used for the first time by Catani in 2012 [50], previous researches had demonstrated the existence of this tract [51, 52]. The FAT connects the pre-­ supplementary motor area (pre-SMA) and the supplementary motor area (SMA) located in the posterior portion of the superior frontal gyrus to the inferior frontal region, especially the pars triangularis and pars opercularis [53]. This tract has an oblique trajectory and is located just medial to the AF and immediately lateral to the corona radiata (Fig. 16.7). The FAT is related to both language and motor control. Imaging studies have shown that the left FAT connections are associated with controlled lexical and phonological selection/retrieval in many linguistic domains, including understanding sign language and gesture. It is also related to executive function/inhibitory control [49]. When the left FAT is stimulated during surgery, speech arrest is generated, a symptom also present in patients whit lesions involving the SMA [54].

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Fig. 16.7 (a) The frontal aslant tract (FAT) connects the pre-supplementary motor area (pre-SMA) and supplementary motor area (SMA) (BA 6) in the superior frontal gyrus with the pars triangularis and pars opercularis in the inferior frontal gyrus (BA 44 and 45). (b) The FAT has been highlighted in yellow. It has an oblique trajectory from the superior frontal gyrus to the inferior frontal gyrus and passes medially to SLF-II perpendicular to this one. (c) DTI 3D reconstruction of the FAT on the directional color map demonstrating its general appearance. (d) Reconstruction of the FAT on the left hemisphere. It has an oblique trajectory connecting the posterior aspect of the superior frontal gyrus with the pars triangularis and pars opercularis in the inferior frontal gyrus. (e) T1 coronal plane MRI with DTI fiber tracking superposition of the left PAT showing the trajectory of this bundle connection of the SFG and IFG. (f) 3D reconstruction of the left hemisphere with the AF (green) and the PAT represented. These two tracts have similar terminations on the IFG

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Middle Longitudinal Fasciculus The temporal pole and parietal lobe are linked by the middle longitudinal fasciculus (MdLF) that lies within the superior temporal gyrus (STG). Some previous studies were unable to isolate the fibers of the MdLF [26, 32], although more recent papers based on DTI tractography and fiber dissections have demonstrated its course and anatomical relationships [34, 55]. The MdLF fibers originate in the STG at the level of the temporal pole and direct posteriorly and laterally. It also receives a contribution from the transverse temporal gyrus. When it gets in the temporoparietal junction, the MdLF makes a wide-angle turn and redirects the trajectory of the fibers from the anterolateral (temporal region) to posteromedial (parietal region) and ascends to reach the superior parietal (precuneus) and occipital regions (cuneus) [55] (Fig. 16.8). The MdLF is located between the AF terminations on the STG, laterally situated, and the fibers of the inferior fronto-occipital fasciculus, situated just medial to the MdLF. At the inferior parietal lobule level, the MdLF is situated lateral to the claustrocortical projection fibers that form the dorsal external capsule. The function of the MdLF is still unclear. Some argue that this tract can be divided into an anterior segment from the temporal pole to the posterior insular point and a posterior segment, from the posterior insular point to its terminations in the parietal region [34]. In this view, the posterior segment would be associated with language [56]. However, this bundle does not have a clear left lateralization, a common feature in language-related fiber tracts [56]. Indeed, a study involving eight subjects that underwent awake craniotomy for resection of gliomas involving STG demonstrated that DES of this tract does not induce language impairments during surgery and the resection of parts of the MdLF did not cause permanent language deficits [57]. As the MdLF connects the STG with the superior parietal lobule, a multisensory processing center, it has been proposed that this tract might be involved in auditory processing acting as the “dorsal auditory pathway” or “where pathway” [55] as proposed by the dual-stream auditory model [21, 58].

Inferior Fronto-occipital Fasciculus Situated medially to the MdLF, the inferior fronto-occipital fasciculus (IFOF) links the frontal lobe to the posterior part of the parietal and occipital lobes. It is a long association fiber tract that forms the ventral external capsule together with the uncinate fasciculus, while the dorsal external capsule is composed of the claustrocortical fibers [32, 34, 59] (Fig. 16.9). The frontal terminations of the IFOF include the middle part of the middle frontal gyrus (prefrontal cortex), pars orbitalis, and pars triangularis. It then directs posterior and inferiorly, deep to the anterior third of the superior limiting sulcus and the superior half of the anterior limiting sulcus to reach the limen of the insula, where it

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Fig. 16.8  The middle longitudinal fasciculus (MdLF) connects the superior temporal gyrus (STG) with the superior parietal region. (a) Illustration demonstrating the connections of the MdLF. This tract connects the superior temporal gyrus (BA 38 and BA 22) with the superior parietal lobule (BA 7) and cuneus (BA 19). (b) Fiber dissection of the left hemisphere. The short association fibers of the temporal, parietal, and posterior frontal lobes have been removed, showing the long association fibers. The MdLF can be seen occupying the STG and running posterior and superiorly when it becomes medial to the temporal terminations of the AF and SLF components. (c) The AF and insular cortex have been removed, demonstrating the trajectory of the MdLF that crosses the SLF-II, being medial to it in the parietal region, and finally reaches the superior parietal lobule. (d) T1 MRI in axial and sagittal planes with superposition of the 3D-reconstructed MdLF showing its terminations on the STG and superior parietal lobule. (e) Left hemisphere 3D reconstruction with a representation of the MdLF (blue), SLF-II (green), and IFOF (red). The MdLF is located lateral to the IFOF in the temporal lobe. When it achieves the inferior parietal lobule, it has a superior and medial trajectory passing medial to the SLF-II and finally reaching the superior parietal lobule

has a shorter diameter. It then passes deep to the middle third of the inferior limiting sulcus, getting in the superior and middle temporal gyri. At the middle temporal region level, the IFOF runs in the roof of the temporal horn, superior and lateral to

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Fig. 16.9  The inferior fronto-occipital fasciculus (IFOF) is a long association fiber tract that connects the frontal lobe to the posterior parietal region and occipital lobe. (a) Illustration demonstrating the connections of the IFOF. The frontal connections of the IFOF include the pars opercularis (BA 44), pars triangularis (BA 45), pars orbitalis (BA 47), superior frontal and middle frontal gyri (BA 8, BA 9, BA 10), and orbitofrontal region (BA 11). The posterior terminations of the IFOF include the calcarine sulcus and cuneus (BA 17), superior and middle occipital gyri (BA 19), superior parietal lobule (BA 7), and fusiform gyrus (BA 37). (b) Fiber dissection of the left hemisphere, SLF, AF, and MdLF has been removed, exposing the ventral external capsule composed of the IFOF, superiorly, and the uncinate fasciculus (UF) inferiorly. The claustrocortical projection fibers that form the dorsal external capsule were removed, exposing the putamen; the posterior portion of putamen was resected, exposing the globus pallidus. (c) Fiber dissection of the left hemisphere in a closer view. The U-fibers and UF have been removed, exposing the terminations of the IFOF in the inferior frontal gyrus. The dorsal claustrum and the dorsal external capsule are viewed superiorly located to the IFOF. In the anterior temporal region, the inferior longitudinal fasciculus (ILF) is exposed. It is laterally located about the IFOF. (d) The central core of the left hemisphere has been dissected. The corona radiata fibers are located superiorly to the basal ganglia. The putamen has been removed, and the anterior half of the globus pallidus enables the visualization of the internal capsule fibers. The anterior commissure can be seen. A commissural fiber tract crosses the midline just inferior to the anterior limb of the internal capsule and then gains the temporal lobe, having a medial position to the IFOF. The ventral external capsule is seen. It is formed by the IFOF dorsally and UF ventrally. (e) T1 MRI in axial and sagittal planes with DTI fiber tracking of the IFOF superposed demonstrates this tract’s regular aspect and its cortical connections. (f) 3D reconstruction of the left hemisphere and the subcomponents of the IFOF. The IFOF is segmented in a ventromedial subfascicle (green), a ventrolateral subfascicle (red), and a dorsomedial subfascicle (blue)

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Fig. 16.9 (continued)

the optic radiations and medial to the MdLF and AF. It continues backward, laterally to the lateral surface of the atrium to reach the parietal and occipital lobes [34, 59, 60]. The posterior terminations of the IFOF include the superior parietal lobule, superior and middle occipital gyri, calcarine sulcus, and fusiform gyrus [59, 61]. Based on fiber dissection, Martino et al. argue that the IFOF has a dorsal and superficial segment and a ventral and deeper segment [59]. Indeed, in a posterior study utilizing both fiber dissection and DTI-based tractography, Sarubbo et  al. detailed the frontal cortical terminations of these two segments as the dorsal IFOF connects the pars triangularis and opercularis to Wernicke’s area, fusiform gyrus, superior parietal lobule, and occipital lobe. The ventral IFOF connects the pars orbitalis, middle temporal gyrus, and dorsolateral prefrontal cortex to the same distal terminations of the dorsal IFOF [62]. Based on a diffusion spectrum imaging-based tractographic study, Panesar et al. proposed that IFOF is divided into three subfascicles according to their spatial orientation within the IFOF bundle: I. Ventrolateral: originating from the pars opercularis, pars triangularis, and pars orbitalis. It remained superficial throughout its course through the external capsule and into the parietooccipital cortex. II. Dorsomedial: originating from the superior frontal and middle frontal gyri, traveling deep to the ventrolateral subfascicle and assuming a fan-like frontal arrangement. III. Ventromedial: originating from the medial, lateral, anterior, and posterior orbital gyri which assumed a deep-and-ventral course in respect to the other subfascicles [61]. The IFOF forms the principal component of the ventral semantic pathway. It has been noted that DES of this tract induces semantic errors during awake craniotomies [60, 62, 63]. Regarding the frontal cortical terminations of the IFOF, stimulation of the pars triangularis and middle and posterior superior temporal gyri induces semantic paraphasia. At the subcortical level, semantic paraphasia was constantly

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induced when stimulating the course of the IFOF in the posterior orbitofrontal area, at the level of the limen insulae, in the posterior part of the temporal stem, and at the floor of the external capsule [63]. On a lesion-based study, Han et al. conclude that the superficial layer of the IFOF may support bridging the semantic memory with the verbal system. The deep layer of the IFOF may be critical for object semantic processing [64]. Other language functions also have been attributed to the IFOF, such as reading and writing [7]. Also, the right IFOF is involved in non-verbal semantic cognition [65]. Duffau et al. argue that the semantic ventral stream is divided into a direct pathway represented by the IFOF and an indirect pathway, composed of the inferior longitudinal fasciculus (ILF), which relay on the uncinate fasciculus (UF), that, in turn, transmits information from the temporal pole to the inferior frontal region [23]. This theory assumes a degree of subcortical plasticity within the network, as the function of the indirect pathway (ILF and UF) may be compensated by the IFOF in the case of damages to UF or ILF. It is observed in patients that underwent anterior temporal lobectomy during epilepsy surgery [23, 66].

Inferior Longitudinal Fasciculus The inferior longitudinal fasciculus (ILF) connects the temporal pole to the dorsolateral occipital cortex. It is located mainly within the inferior and middle temporal gyri and runs laterally and inferiorly to the temporal horn of the ventricle. At the level of the paraoccipital notch, it bends upward to be distributed to the dorsolateral occipital cortex, not reaching the calcarine sulcus (Fig. 16.10) [34, 67]. The curse of the ILF is lateral to the IFOF in its anterior part and then directs medially, becoming interconnected with IFOF fibers [32]. Panesar et al., in a recent paper, found that ILF is also divided into two different subfascicles, a dorsal and a ventral one [68]. The authors found that the dorsal subfascicle connects mainly the middle and superior temporal gyri with the superior occipital gyrus. On the other hand, the ventral ILF, a generally less robust bundle, links the superior, middle, and inferior temporal gyri with the lingual gyrus [68]. The ILF is recognized as a multi-functional tract involved in a broad range of brain functions concerning the visual modality, including object, face, and place processing, reading, lexical and semantic processing, emotion processing, and visual memory [69]. Regarding its subcomponents, it is argued that the dorsal ILF subserves both semantic, spatial, and facial recognition tasks and the ventral ILS is involved in visual recognition tasks [68]. ILF, together with the uncinate fascicule, is implicated as part of an indirect semantic pathway. Indeed, electric stimulation of this tract during surgery elucidates semantic paraphasias [23, 67].

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Fig. 16.10  The inferior longitudinal fascicle (ILF) connects the temporal pole to the occipital lobe. (a) Illustration demonstrating the inferior cortical connections of the ILF. This tract connects the temporal pole (BA 38) to the occipital region and lingual gyrus (BA 18 and BA 19). (b) Fiber dissection of the left hemisphere. The cortex and U-fibers of the basal surface of the temporal lobe have been removed. The terminations of ILF can be seen in the anterior temporal pole and lingual gyrus. (c) Lateral view of the ILF. The ILF fibers have an anterior to posterior direction connecting the temporal pole to the superior and middle occipital gyrus and lingual gyrus. (d) 3D reconstruction of the left hemisphere and ILF subsegments. The ILF is composed of a dorsal component (red) that connects the temporal pole with the occipital lobe and a ventral segment (green) that mainly finishes at the lingual gyrus. (e) 3D reconstruction of the left hemisphere demonstrating the relationship of ILF (green and red bundles) and IFOF (yellow bundle). Both subcomponents of the ILF are laterally located to the IFOF, reaching more superior regions than ILF. (f) Oblique view of the left hemisphere on an MRI-based 3D reconstruction. The components of the ventral external capsule were rendered to demonstrate their relationship with ILF.  The IFOF (green) connects the frontal lobe with the occipital region, having standard posterior terminations with the ILF. The UF (red) terminates at the temporal pole, medial to the ILF (blue) temporal pole terminations

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Uncinate Fasciculus The uncinate fasciculus (UF) is a frontotemporal association tract as it connects the anterior temporal region with the orbitofrontal area of the inferior frontal gyrus [32, 34]. It runs along the limen of the insula, inferiorly situated to IFOF, and forms with this one the ventral external capsule. After it crosses the limen of the insula, it penetrates in the ventral portion of the temporal stream, which is formed by the white matter of the three temporal gyri [70] (Fig. 16.11). Given the UF cortical connections, this tract has been implicated in emotional processes. Damages to UF are also related to psychiatric disorders [71, 72]. The role of UF on language is still unclear. Although the DES of this tract during awake craniotomies did not induce language disturbances, and its resection did not implicate permanent language deficits [70], some argue that the UF damage results in a

b

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Fig. 16.11  The uncinate fascicle (UF) is a C-shaped fiber tract that connects the inferior frontal lobe with the temporal pole. (a) Illustration demonstrating the cortical connectivity of the UF. The UF mainly connects the orbitofrontal region (BA 47) and the temporal pole (BA 38). (b) Fiber dissection of the left hemisphere with an emphasis on the ventral internal capsule. The UF is located in the ventral aspect of the IFOF, and its frontal terminations are also inferiorly located to the IFOF frontal terminations. The dotted line separates the fibers of IFOF that have a posterior course from the UF fibers, which have a curved course to reach the temporal pole. (c) MRI-based 3D reconstruction of the left hemisphere with a 3D reconstruction of the UF based on DTI fiber tracking. The UF reaches the anterior portion of the orbitofrontal gyrus and the temporal pole. It passes through the ventral portion of the limen of the insula. (d) Fiber tracking of the components of the ventral external capsule: IFOF (green) and UF (red), the three-dimensional reconstruction of the left hemisphere was also added to demonstrate the relationship of these tracts with the cortical anatomy

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impaired proper name production [73]. Indeed, the UF is accepted as a subcomponent of the indirect ventral semantic pathway that can have its functions executed by the IFOF in the case of damages, a typical example of subcortical plasticity [23, 70].

Conclusion Since Broca and Wernicke made their contribution to the understanding of language processing, the concepts underlying this matter have developed significantly. The incorporation of new neuroimage methods such as DTI tractography, functional MRI, and magnetoencephalography has improved the comprehension of the language network. Also, the consolidation of brain mapping methods in patients who underwent awake craniotomies has contributed to the elucidation of the specific function of each subcomponent of the language network. The evolution of the human language model has changed from a more localizationist model as proposed by the pioneers to an hodotopic framework [17, 18, 23], which gives the same importance to cortical regions and subcortical tracts of white mater. Indeed, the human language demands several high-order processes occurring

Fig. 16.12  Illustration representing the subcortical distribution of the primary long association fibers of the left hemisphere in the coronal plane. The SLF-I is located in the medial surface of the superior frontal gyrus above the cingulum. The SLF-II is located in the deep portion of the middle frontal gyrus and the SLF-III within the inferior frontal gyrus. The AF ventral and dorsal lie in between the SFL-II and SFL-III, in the frontoparietal operculum. In the temporal lobe, the MdLF is located in the superior temporal gyrus, and the ILF mainly in the inferior temporal gyrus. The UF has terminations in the amygdala, in the medial portion of the temporal lobe. The IFOF is located laterally to the optic radiations positioned in the lateral aspect of the temporal horn of the lateral ventricle

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at the same time. Executing and understanding speech is possible given a complex and intricate network of cortical and subcortical regions of the brain. The involvement of primary and secondary language centers and tracts represents a challenge for neurosurgeons, neurophysiologists, and multidisciplinary teams who faces conditions such as LLG. In fact, it has been shown a high incidence of gliomas in language-related areas [3]. In this scenario, understanding the language anatomy under a more functional view has allowed the use of brain mapping in cases where the language is at risk, which has improved both resection grades and quality of life [74]. The general architecture of this network and its components were discussed here (Fig. 16.12). Given the constant evolution of techniques used to explore the white matter tracts, several controversies have been raised in this matter. The morphology and the precise anatomy of the white matter tracts are still not entirely clarified. In this chapter, a more anatomical approach was used. A focus was made in explaining the general anatomy of the white matter tracts related to language, the cortical regions linked by each tract, and its course within the brain. For those who intend on ingressing in the field of brain mapping, the knowledge of the anatomy of the cortical and subcortical sites associated with language is paramount. For an appropriate brain mapping, the team should incorporate a dynamic view, where a given function would be not confined to a specific brain region, especially for patients with slow-growing lesions [75]. The plasticity of cortical regions is recognized [76, 77]. Although white matter has a plasticity potential in adulthood [78], it is significantly limited compared to the brain cortex [79]. Therefore, surgical resections should be made according to individual anatomofunctional organization of the language networks, respecting functional boundaries, consequently leading to the optimization of the benefit/risk ratio of surgical procedures [80].

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Chapter 17

Awake Surgery: Performing an Awake Craniotomy Silvia Mazzali Verst, Juliana Ohy, Cleiton Formentin, and Marcos Vinicius Calfat Maldaun

Abbreviations CC Corpus callosum CNS Central nervous system DES Direct electrical stimulation DTI Tractography ECoG Electrocorticography EOR Extent of resection FLAIR Fluid-attenuated inversion recovery GBM Glioblastoma GTR Gross total resection HF High frequency

Supplementary Information The online version contains supplementary material available at [https://doi.org/10.1007/978-­3-­030-­95730-­8_17]. S. M. Verst (*) Instituto de Ensino e Pesquisa (Research and Educational Institute) of Sírio Libanês Hospital, São Paulo, Brazil Brain Spine Neurofisiologia, Jundiaí, SP, Brazil J. Ohy · C. Formentin Researcher at Instituto de Ensino e Pesquisa (Teaching and Research Institute) of Hospital Sirio Libanês, São Paulo, SP, Brazil M. V. C. Maldaun Instituto de Ensino e Pesquisa (Teaching and Research Institute) of Hospital Sirio Libanês, São Paulo, SP, Brazil Neurosurgery Department, Hospital Sirio Libanês, São Paulo, São Paulo, Brazil © The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 S. M. Verst et al. (eds.), Intraoperative Monitoring, https://doi.org/10.1007/978-3-030-95730-8_17

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HFC High functional connectivity IDH Dehydrogenase gene iMRI Intraoperative magnetic resonance imaging IOM Intraoperative neurophysiology monitoring ioUS Intraoperative ultrasound LF Low frequency LLG Low-grade glioma MEG Magnetoencephalography MEP Motor evoked potential MGMT O6-methylguanine-DNA methyltransferase NF Neurophysiologist OMFTCT Ohy-Maldaun Fast Track Cognitive Test ON Object naming VMLA Verst-Maldaun Language Assessment

Introduction Initially, awake craniotomy was planned to help epileptic focus resection in Montreal Neurological Institute and Hospital by Wilder Penfield. Medical search for language function understanding goes back to Broca, who in 1861 showed that a small area of left hemisphere had the power of speech (cited by Penfield [1]). George A. Ojemann developed language tasks to be performed during DES of the brain and standardized the awake approach, being pointed as the father of the modern awake craniotomy. Hugues Duffau extensively investigated intraoperative proper language and cognitive tasks and keeps pushing us forward to new concepts and frontiers in connectivity and neuroplasticity. Unfortunately, it is not the scope of this chapter to commemorate all the incredible researchers of the last century. But we have to mention Brazilian pioneer Professor Raul Marino, who learned directly from Penfield (more details in Chap. 1). A PubMed search using the terms “language,” “brain,” and “mapping” comprising the period from January 1, 1959, until May 20, 2021, resulted in 10,710 results. There was a slowly growing curve concerning the amounts of publications in the subject in the first 37 years. It jumped to over 100 papers per year in 1997. And in 2015, a record was achieved with 777 papers on this subject that year. Therefore, since Wilder Penfield mapped the brain using an electrical protocol of 2.5 ms pulse duration at 1 V and 60 pulses per second (60 Hz) in 1959 and found out “an interpretative cortex in temporal lobe” [1], awake craniotomy has evolved greatly. Penfield was a visionary ahead from his time. With brain mapping, he discovered specific brain function in different cortical areas: motor and sensory (1937), language (1949, 1952, and 1959), and supplementary motor area (1951) [2]. Nowadays, awake craniotomy is a complex teamwork that demands proper training.

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General Concepts Presented by the Neurosurgeon Low-Grade Glioma Surgery Low-grade gliomas (LLGs) are known for their diverse pathology and clinical behavior and account for 17% to 22% of all primary brain tumors [3–5]. The natural growth rate of LGGs is believed to be linear regarding diameter and to progress approximately 4  mm/year [6], ultimately evolving to high-grade glioma. Unlike solid tumors, for which exponential or geometric growth represents expansion of volume, gliomas consist of motile cells that can migrate through white matter pathways as well as proliferate [6]. At an unpredictable point of time, LGG speed of growth increases due to malignant transformation, a key clinical event that leads to increased morbidity and premature death [7]. Recent understandings into the molecular biology of LGG with the discovery of isocitrate dehydrogenase (IDH) gene and 1p19q codeletion and their impact on survival have led to a recent reclassification of gliomas, by incorporating molecular parameters [3]. Median survival for patients with LGG ranges from 5.6 to 13.3 years and is dependent on specific histology and molecular characteristics [8]. Treatment options include surgery, radiotherapy, and chemotherapy. In 2012, a Norwegian study including patients with LGG showed that early surgical resection was associated with better overall survival than biopsy and watchful waiting [9]. Surgical intervention is generally performed with the goal of maximum safe resection and aids in diagnosis by providing tissue for molecular testing [10]. Gross total resection (GTR) is significantly associated with decreased mortality and likelihood of progression at all time points compared to subtotal resection [10]. Moreover, a supratotal resection, i.e., a wide resection with a margin beyond MR imaging abnormalities, ideally with 2 cm of margin around the diffuse LGG visible on MRI, can dramatically change the natural history of LGG by delaying the risk of malignant transformation [11].

Glioblastoma and Extent of Resection The role of surgery in the treatment of glioblastoma (GBM) has been considerably studied. The concept of resection changed from those arbitrary categories (gross total, subtotal, and partial) into the new model of maximal and safely achievable volumetric resection. A study from the University of Texas on 416 patients with newly diagnosed and recurrent GBM demonstrated that overall survival significantly increases with each unit increase in the extent of resection (EOR), starting from 89%, with the strongest effect of resection on survival being achieved at the 98% threshold [12]. Later, a University of California study including 500 patients with GBM showed a significant survival advantage starting at 78% EOR, and an EOR ≥ 95% had the greatest impact on overall survival [13]. However, its already

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known that GBM is as an invasive tumor and the area outside the contrast-enhanced region on a T1-weighted MRI is usually infiltrated by tumor cells [14]. Fluid-­ attenuated inversion recovery (FLAIR) images represent these invasive cells. There are some evidence that additional removal of a significant portion of the FLAIR abnormality region, when safely feasible, may result in the extension of survival without significant increases in postoperative morbidity [14]. A recent JAMA study confirms association between maximal EOR and overall survival for the contrast-­ enhanced tumor in all molecular subgroups, and, in younger patients, the additional maximal resection of non-contrast-enhanced tumor, regardless of IDH and O6-­ methylguanine-­DNA methyltransferase (MGMT) status [15].

“Safe” Resection Glioma surgery is a delicate balance between achieving maximal tumor resection and inducing new deficits. Surgically acquired motor and language deficits may have a negative impact on survival and quality of life in GBMs’ patients [16]. Those patients were less likely to receive normal-fractioned radiotherapy and chemotherapy [16]. In this context, to maximize contrast-enhanced and non-contrast-enhanced resection, advanced intraoperative imaging methods and fluorescence-based tumor biomarkers can be used, whereas direct electric stimulation (DES) will help to decrease perioperative morbidity. Considering tumors in apparent functional areas, mapping of language and sensorimotor function is the gold standard to achieve maximal safe resection [17–21]. Since the original description of awake craniotomy by Horsley, this technique has been used for different indications with the predominant aim of improving safety [22]. Different techniques have been described in the literature for the testing and identification of functional sites [23–25]. DES during awake surgery allows the identification of eloquent functional cortex, and it is applicable for lesions arising in different locations in the brain. Indeed, awake craniotomy is associated with low complication and mortality rates, as well as low resource utilization [26–28]. However, it is used in just around 20% of glioma surgeries [18, 29]. A meta-analysis examining the usefulness of DES in glioma surgery revealed that mapping is associated with twofold reduction in late severe neurologic deficits compared to surgery without DES.  Yet, there might be an increase in temporary early severe deficits [18, 30].

“Maximal” Resection The importance of maximal safe resection in gliomas supports the use of different tools to increase the EOR during surgery, like intraoperative magnetic resonance imaging (iMRI), 5-ALA, intraoperative ultrasound (ioUS), and neuronavigation. iMRI has been used for more than a decade intending to accomplish better results in the EOR of gliomas. EOR of contrast-enhancing lesions might be improved by

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iMRI, since this technique can show contrast-enhancing tumor on the surgical cavity as well as underneath it (T1, T2, and T1 w/ gadolinium). Also, awake craniotomy can be safely performed in a high-field (1.5 T) iMRI suite to maximize tumor resection in eloquent brain areas with an acceptable morbidity profile at 1 month [31]. However, it requires an interruption of the surgery for acquisition of the images, and, therefore, it’s a time-consuming method. 5-ALA offers the possibility to detect fluorescent tumor tissue in the cavity through the microscope in a real-time way. The use of 5-ALA has a rational extra cost and is possible without complex equipment. An analysis of residual tumor, total resections, and neurological outcomes comparing iMRI and 5-ALA demonstrated that iMRI may be significantly superior to 5-ALA for GBMs at comparable periand postoperative morbidities [32]. ioUS is a compact and portable system, widely available, that can independently provide real-time imaging during brain surgery. It has a significant advantage over the other intraoperative aids for image guidance, especially in terms of cost and adaptability to different clinical scenarios. On the other hand, ioUS is user dependent, with a steep learning curve. Neuronavigation system is crucial for planning a tailored craniotomy in glioma surgery, whereas shifts in the position of the brain or tumor related to resection may cause critical errors in navigational data [33]. It is recommended to associate neuronavigation to brain mapping techniques, which performs a functional assessment of the exposed tissue.

Case Selection Suitable patient selection is essential to ensuring intraoperative success with awake mapping. Awake craniotomy should be considered in all patients with supratentorial lesions that are in or adjacent to eloquent areas, although other groups have utilized the technique non-selectively for supratentorial tumors [28]. A full assessment of a patient’s clinical history, medical comorbidities, neurological deficits, psychiatric disorders, and seizure frequency should be taken into consideration when formulating the operative plan. In our experience, there are few absolute contraindications to awake craniotomy, as unwillingness of the patient and claustrophobia. We have adopted some maneuvers to alleviate most potential problems: (a) patients with a psychiatric history were treated preoperatively with antidepressant medications; (b) patients with significant mass effect were offered a staged procedure or initial internal debulking, followed by awake mapping; (c) intraoperative seizures were treated with iced saline’s solution applied to the cortex during stimulation; and (d) patients with severely impaired preoperative function underwent a staged procedure. Previous tumor resection limited by positive mapping should not preclude awake surgery, because the adult central nervous system (CNS) reorganizes motor and language areas in patients with glioma. This neural plasticity results in up to 25% of previously identified sites no longer demonstrating eloquence at a repeat surgery [23, 34]. We always should concern that the main principles of modern

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neurosurgical oncology are (1) accessibility (ability to reach the tumor using anatomical references, navigation, and ioUS); (2) resectability (ability to remove the tumor using microsurgical skills, ioUS, IMRI, and 5-ALA); and (3) preservation of quality of life (improving physical and emotional performance of your patient during adjuvant therapies, like radio- and chemotherapy). To reach these goals, functional-­anatomical understanding, awake craniotomy, and intraoperative neurophysiology monitoring (IOM) are crucial.

Perioperative Evaluation Preoperative imaging includes MRI with and without gadolinium, and diffusion tensor imaging (DTI) for white matter pathways (corticospinal tract, superior longitudinal fasciculus, arcuate fasciculus, uncinate fasciculus, inferior orbitofrontal fasciculus, optic pathways) Functional MRI (fMRI) may be included if available. However, these preoperative imaging techniques are insufficient to accurately exclude function and should therefore not be used to justify asleep surgery [23]. Although useful for determining laterality of language, these techniques are insufficient to determine the exact location of functional areas and may not effectively distinguish between involved and essential language locations. Compared with DES, fMRI had a sensitivity and specificity, respectively, of 91 and 64% in Broca’s area, 93 and 18% in Wernicke’s area, and 100 and 100% in motor areas [35]. Therefore, DES was significantly more accurate compared with fMRI in demonstrating functional speech areas [35]. Preoperative magnetoencephalography (MEG) measures high functional connectivity (HFC) network sites. Its role in functional language connectivity evaluation is still sparse. Identifying HFC sites might assist with preoperative planning and improve intraoperative safety. Mitchel Berger, 2021, resected DES-negative HFC sites during surgeries for low- and high-grade gliomas. The patients evolved a transient language impairment for naming and syntax that resolved in 6  months. Therefore, MEG seems to be useful regarding patients’ counseling about postoperative risk and assisting with preoperative surgical planning [36]. There is an unpredictable shifting of major white matter tracts during surgery. The real position of functional cortex and tracts may differ by more than 1 cm from that predicted by neuronavigation. The use of intraoperative mapping techniques can overcome this situation [37]. Preoperative clinical evaluation includes baseline language and sensorimotor test performed 24–48 hours prior to surgery. Although there is no guideline, preoperative deficits may hinder intraoperative testing if the previous object naming (ON) error rate ranges between 10% and 25% [19]. Pre-op assessment is relevant for obtaining comparative data for the next phases. The patient gains confidence, feeling trained for the intraoperative testing [38]. In addition, it is during this phase that the neuropsychologist creates a bond with the patient and his/her family. Doing so, the next steps will be carried out with greater overall acceptance.

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Language assessment is further applied before hospital release and 30 days after release. It allows a more precise estimation of patient’s cognitive status and aims to minimize long-term bad outcome [39]. The before-hospital release evaluation takes place usually 3 days after the surgery in non-complicated cases. Due to the fact that the patient is recovering from the surgical procedure, the applied tasks have a lower level of difficulty. Yet, all cognitive functions are tested in the same way as in the preoperative phase. At this point, the diagnosis of patient’s cognitive status is important to better understand intraoperative behavior and to plan rehabilitation, if needed. During the 30th-day follow-up, the patient is checked for any significant cognitive impairment. He/she will receive his/her neuropsychologic discharge or will be referred to continue his/her cognitive rehabilitation. Language protocols vary among institutions. For perioperative testing, we created Ohy-Maldaun Fast Track Cognitive Test (OMFTCT), already under Portuguese native speakers’ validation. It aims to assess patients’ cognitive functions completely and briefly, consisting of ten subtests: naming, verbal memory, semantics, calculation, spelling, visual memory, reading, syntax, drawing, and spelling. Each task is composed of 5 items that score 1 point each, with a total score of 50 points. Some cognitive tasks, like calculation and object naming, might be combined with a simultaneous motor test (e.g., static or dynamic body balancing, walking, limb movement), composing a dual task. OMFTCT was created from the database images used by Verst-Maldaun Language Assessment (VMLA) [40], made for intraoperative testing (see details in Chap. 18). In order to universalize testing and to enable access to free language tests, OMFTCT and VMLA can be freely accessed at vemotests. com. Figure  17.1 illustrates a case, showing perioperative scores and intraoperative tasks.

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INTRAOPERATIVE ASSESSMENT Initial cortical mapping (To4, ISI 2, 0.5ms, 10 mA, 2Hz): VMLA-ON: with DES: 1 to 22: negative VMLA-Semantic:_with DES: S1-S19: negative During resection: - Repetition of a sequence of 3 words (3-4 syllables): ok - Sentences formation: ok - Word formation: ok Subcortical mapping and resection by pars triangularis and opercularis: VMLA-ON: with DES: reverberation 4-9, 1-33, 2-37 and 6-2 Without DES: VMLA- Semantic: S20-S42: hesitation at: S23 and S42 VMLA-ON: 23 objects: no errors

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Fig. 17.1  Man, 41 years old, left frontal glioma. Complaining from memory impairment. By preoperative Ohy-Maldaun Fast Track Cognitive Test: verbal memory 3/5, a score that precludes intraoperative testing of this function. Patient was mapped and monitored during tumor resection. Initial cortical mapping: negative. Positivity was observed at subcortical level with DES and by resection during object naming and semantics

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One of the most helpful features of OMFTCT is that it can be applied during hospitalization by the neuropsychologist, the medical resident, or the neurosurgeon. Application takes no longer than 1  hour, which increases patient compliance. Usually, other standard language tests demand long testing, being stressful and tiring to the patient. OMFTCT is usually effective in most of our cases, but there are patients that need to be submitted to a complete neuropsychological assessment, for more detailed diagnosis. The combination of intraoperative language tasks will depend on the side and anatomical tumor location and patient’s hand dominance. The language network is more complicated and integrated than historically considered, and the location of essential language sites can be extremely variable and difficult to predict preoperatively, far beyond “Broca’s” and “Wernicke’s” areas [36, 41]. Speech arrest is most frequently evoked in the pars opercularis or precentral gyrus but can also be found throughout the frontal operculum and temporoparietal region [41] (details in Chap. 18).

Awake Surgery: Technical Nuances A skilled neuroanesthesiologist is paramount for a successful awake craniotomy. We prefer the “asleep-awake” technique (details in Chap. 15). A craniotomy is performed to expose the cortex corresponding to the tumor area and a limited amount of surrounding tissue. Dural manipulation can be painful, so copious irrigation is required during craniotomy, and a dura mater block is performed using a 30-gauge needle with 1% lidocaine to infiltrate the region around the proposed dural incision. The dura is opened in a manner that best suits an ideal exposure of the lesion. Once the dura mater is opened, the patient is gradually awakened by suspending the administration of all medications. Upon opening the dura, the brain is assessed for swelling, which could be overcome by asking the patient to perform controlled hyperventilation. If an unacceptable degree of brain swelling occurs after durotomy, additional mannitol may be given, the head of the bed raised, and the arachnoid space opened for the release of CSF as additional maneuvers. Mapping begins after patient’s wakefulness. Irritation of the middle fossa floor during resection may cause pain or elicit the trigeminocardiac reflex, causing nausea, vomiting, hypotension, and bradycardia [23]. Initial cortical mapping is used to identify negative speech and motor regions, allowing the entrance of the cortical area [42]. Considering the variability across patients, subcortical mapping is virtually always required for safely identification of the language network. DES can detect eloquent structures by inducing a transient virtual lesion based on the inhibition of a circuit, identifying with great accuracy and reproducibility the structures that are crucial for language.

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Electrical stimulation (either bipolar or monopolar) is usually applied manually with a handheld probe. Electrocorticography is required to monitor for epileptic events and discharges [23, 43].

Brain Mapping from the Technical Point of View Language function is based on interaction between different neuronal circuits. Theoretically, a disturbance at any point of a connected cortical-subcortical pathway could manifest clinically as symptom from a related cortical area. This phenomenon is called hodotopy [44, 45] (Fig. 17.2). This feature might be reproduced by DES, in which any focal blockage produced at a point of a tract could interrupt the function at any cortical area related to this point [45]. For instance, a patient with a tumor in the posterior temporal region may have spelling difficulty due to impairment of the U-fibers that connect temporal cortex to inferior parietal gyri. Preferably, we perform the awake technique only for language mapping demanding cases. In our routine, the neurophysiologist (NF) applies the cognitive tasks and manages the IOM, due to cost optimization. Usually, a technician operates the IOM system.

Fig. 17.2  Hodotopy: cortical-subcortical interconnections form an inter-dependent network. It can be disrupted by focal disease or stimulation at subcortical level (points 1 and 2) resulting in the disruption of related cortical function (points A, B, or C). Disconnection syndrome, topographic dysfunction, or both could arise from this focal blockage. (Catani, M and de Schotten, MT 2012; [45])

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Fig. 17.3 (a, b) Tablet positioning solutions, depending on patient’s face exposure. Positioning of the tablet must attend patients’ need of fully watching the screen. The tester must have access for any needed adjustments and to switch between tests

Positioning the patient and the tablet for language task demands all team cooperation. Figure 17.3 shows possibilities of tablet fixation adapted to patient’s face exposure. Usually, the tablet is placed soon after the neuronavigation setup. During the awake phase, the NF sits in front of the patient, to allow better interaction, control unproper movements and quickly identify epileptogenic events’ onset, check on the tablet, and perform dual task. Optimizing the choice of tests is critical since testing takes no longer than 2 hours. Our protocol includes an IOM battery of tests for eloquent area in all patients. It is composed of phase reversal (if the central lobe is reachable), direct cortical motor evoked potential (MEP) using the grid electrode, somatosensory evoked potential of contralateral ulnar and tibial nerves, cortical and subcortical mapping, electromyography, and electrocorticography (ECoG). The reason for the complete IOM protocol relies on the possibility of non-cooperative patient and seizure events that demand sedation. Additionally, preservation of MEP and loss of limb voluntary movement point to a supplementary motor syndrome in frontal approaches. Early identification of epileptogenic events and afterdischarges using ECoG improves patient’s

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management. ECoG should be included in IOM protocol for language and motor cortical and subcortical mapping for safety reasons. Additionally, continuous direct cortical MEP during motor mapping is mandatory. Language tests are continuously performed during tumor resection, alternating with cortical and subcortical mapping as necessary (Figs. 17.4 and 17.5). Monitoring do not replace mapping. Indeed, they should be performed as a complement to each other. By monitoring while the resection goes on, it is possible to identify areas that

Fig. 17.4  Language mapping and monitoring are complementary to each other and should be interspersed. Ongoing cognitive assessment during resection is monitoring. If positivity starts, for example, hesitation, reverberation, and paraphasia, the surgeon re-maps the area. Interchanging mapping and monitoring improves overall safety

Fig. 17.5  Flowchart on how we perform and react during awake craniotomy. Positive mapping identifies areas that should be preserved, while negative mapping sites to be resected. Ongoing language monitoring improves identification of function disruption or “network instability,” and immediate re-mapping is performed

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repeatedly evoke an error, for example, phonemic paraphasia. This situation leads to mapping this area again to identify and preserve eloquent tissue. Assuming the methodology is strictly applied, no false negatives are expected, and brain function will be blocked by DES [46]. This optimal sensitivity justifies why mapping is the gold standard for recognizing reshaped brain modified by slow tumor growth and neuroplasticity. Mapping should not be overlooked. In our practice, when language areas are identified, the resection margin is maintained 1–2 cm away from those cortical areas. Resection is stopped if speech function deteriorates but is restarted if full recovery occurs within 5 min.

Choosing Stimulus Protocol Methodological rigor and the meticulous performance of mapping are fundamental to adequate tumor resection and avoidance of permanent neurological deficits [47]. If the principles are strictly observed, the sensitivity of DES for the detection of cortical and axonal eloquent structures is 100% [46]. Any false-positive or falsenegative stimulation result could lead to erroneous surgeon’s decision-making. Mapping effectiveness is fully dependent on protocol selection and application. It is a complex interplay between stimulation parameters (rheobase and chronaxie), probe characteristics (mono−/bipolar) and positioning according to the orientation to the fiber, and tissue impedance (which varies according to the illness, whether tumor or epilepsy) [46]. The stimulation aims to block the function which leads to clinical error during the language testing. The clinical error points to underlying eloquent tissue (either cortical or subcortical) that needs to be preserved. Functional disturbances should be analyzed by a dedicated person during the awake craniotomy in order to improve their identification. Lastly, by language mapping, it is not possible to estimate the distance between the probe and the tract fiber. Low Frequency (LF) Versus High Frequency (HF) Low Frequency In 1986, Ojemann synthesized his methodology: 1. For ON, image was presented every 3 to 4 seconds. 2. Two positive stimulations in three trails meant eloquent area. 3. Current level should be adequate to block the function, without spreading to distant sites and loosing specificity. 4. “The adequate but localized” current level is the highest one that does not result in afterdischarges in ECoG. 5. Biphasic 1ms-pulse at 60 Hz (LF), bipolar 5 mm-apart tips stimulator, 2–8 mA (one to four times cortical motor threshold).

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6. Once the current level is selected, an arbitrary set of 15–20 points in the vicinity of the lesion is tested (including areas over the lesion and areas supposed to be essential for language) [48]. Ojemann recommended to start with ON task, presenting objects like slides and stimulating every third or fourth item. Procedure should restart as soon as all 15–20 points were done and repeated three times in sequence. Resection should be done while patient was engaged in naming, and as soon as deficits developed, resection must be terminated. Ojemann settled the fundaments for language mapping and monitoring. During asleep approaches, LF pulse duration has reached 2.5  ms by Bergers group and up to 40 mA by Ebeling and his colleagues (cited by Taniguchi et al. [49]). High charges can damage neural tissue and prevent real monitoring. Therefore, long-train stimulation should be avoided. High Frequency The development of high-frequency (HF) technique improved greatly motor mapping under general anesthesia, overcoming a limitation of LF.  Monopolar HF (250–500 Hz) methodology differs from Ojemann’s abovementioned assembly in specific points: 1. Monopolar stimulation blocks a greater number of neural fibers, since stimulus travels from the active toward the reference electrode. 2. Pulse is monophasic and lasts 500uS. 3. Stimulus is anodal for cortex stimulation and cathodal for subcortical. 4. Usually, current level reaches up to 15 mA, and motor evoked responses could be used to settle the proper intensity. Monopolar 250–500 Hz stimulation was proposed by Taniguchi et al. [49], aiming to turn motor pathways continuously monitorable under general anesthesia [49]. They performed direct anodal cortical stimulation, using a constant voltage or constant current stimulator, delivering three to five monophasic square pulses of 200–500uS duration and intensity up to 20 mA. Compound muscle action potentials were recorded in contralateral hand and forearm flexors, without disturbing patients’ movements during microscopy. LF and HF Stimulus Propagation A proper understanding of neural conduction and electrical stimulus parameters is essential for a more comprehensive analysis of effectiveness of both techniques. An accumulation of excitatory postsynaptic potentials is expected after a short train of square pulses is delivered to the first motor neuron using an interstimulus interval (ISI) shorter than 7  msec, at a frequency of more than 150  Hz. Anodal

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cortical stimulation activates pyramidal cells and produces D and I waves [50]. Downward-travelling D waves will active the second motor neuron, even under general anesthesia [51, 52]. The behavior of D waves, i.e., its recovery time and amplitude, is dependent on pulse duration and ISI [51, 52], showed that the best combination is a pulse of 500uS and ISI of 4 ms (250 Hz), resulting in the greatest D2 wave with a recovery time equalizing the ISI value. Of remark, this phenomenon is also seen with an ISI of 20 ms (50 Hz) (Fig. 17.6). Deletis et al. [51, 52], stated that “D1 wave amplitude reflects the amplitude of conducted impulse in each fiber, the number of conducting fibers and synchronicity of their discharge. Each of these properties could vary in the D2 wave as a function of the ISI and contribute to the change in D2 amplitude relative to D1.” ISI directly impacts synchronicity of D2 wave activated population, ultimately impacting stimulus propagation. Hence, LF and HF assemblies share common points: 1. Both were initially used for cortical motor mapping. 2. Both use a pulse of 500μS duration: monophasic pulse for HF and biphasic pulse (anodal-cathodal) of 500μS each one for LF. Yet, only the anodal phase is effective for stimulation [19, 47].

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3. 50 Hz and 250 Hz correspond to ideal ISI for synchronization between D1 and D2 waves. This fact might substantiate the effectiveness of both techniques. 4. Both evoke muscle contraction, which is clonic for HF (primary area activation) and tonic for LF (premotor area activation). 5. Both use constant current because it is safer and independent from tissue impedance. 6. Both block function at language tracts. 7. Stimulation should be applied for around 5 s. Central Nervous System Structural Basis for Stimulus Propagation Neural transmission is a matter of fiber diameter and its conduction velocity. Narrower fibers conduct slower than larger ones. Larger fibers are more often present in long tracts than in shorter ones. Finally, fiber systems have a very constant composition, although differing from each other [53, 54]. Corpus callosum (CC) was shown to be composed of unmyelinated and myelinated fibers, with diameters varying from 1.5 to 5 μ [54, 55]. Szentagothai-Schimert [53], showed a predominance of thinner fibers in uncinate compared to cingulate. Fiber density also varies among CNS tracts. For example, the corticospinal tract has 100,000 fibers per square millimeter, while CC has 300,000 [54]. Refractory periods and fiber diameter of central tracts seem to be related [56]. Szentagothai-Schimert [53], stated that projection, associative, or commissural tracts differ in their fiber thickness composition. This variation could be a matter of interindividual particularities, age, and gender, and there is uncertainty about its functional role. Tipically, tracts are composed of non-myelinated and myelinated fibers of different calibers, rarely thicker than 8 μm with exception to the pyramidal tract (up to 12 μm), ansa lenticularis, thalamus, and olfactory tract [53]. Within a tract, fibers of different calibers combine according to their endpoint connection, as seen by Szentagothai-Schimert for medial lemniscus [50], pointed that 90% of pyramidal tract is composed of slow conduction fibers up to 4 μm and only 1.7% are faster fibers with thickness between 11 and 22 μm. Myelinated fibers correspond to 60–94%. Chronaxie and Rheobase Characteristics of an axon fiber impact its chronaxie, which is longer for non-­ myelinated and thinner fibers [46]. Rheobase (Rb) is the threshold (THR) current at infinite pulse duration that activates an action potential [46, 56, 57]. Chronaxie (Ch) is the time on the intensity-­ duration curve twofold the Rb [56, 57]. Ch is the optimal stimulation intensity to generate an action potential using two times the minimum charge (best benefit/risk ratio) [46]. Optimal THR varies among individuals and results from inherent Rb and Ch, which ultimately depends on pulse duration and stimulus frequency. For single

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pulse stimulation, Rb and Ch were plotted in intensity-duration curves. Ch of human brain white matter using single pulse ranged from 40 to 100uS, while by gray matter ranged from 200 to 700 μs [56]. Hence, the axon can be more easily stimulated than the cell body [46, 56]. Abalkhail et al. [57], studied Rb and Ch using a train of 5 pulses for cortical motor stimulation. They found optimal values to be 200uS pulse duration and ISI of 3 or 4 ms (333 or 250 Hz, respectively) [57]. Brain tissue impedance is a matter of controversy. Kombos and Süss [50], stated that gray matter presents higher resistance (4–6 times more) than white matter. Mandonnet et al. [46], reported that it is higher for white matter (500 Ohms) than for gray matter (250 Ohms) and cerebrospinal fluid (65 Ohms). According to Ohm’s law, impedance influences current flow. Hence, Ch, Rb, and tissue impedance are the physics elements that directly impact THR. DES for language mapping starts with the determination of THR energy needed to block the neuron. Usually, determining the motor THR is easier, and this value can be used for further cognitive and language mapping [20, 47]. High Frequency for Language Mapping The first HF stimulation for language testing was performed using an extraoperative subdural grid followed by intraoperative mapping on the next day [58]. Our language mapping protocol switched from LF to HF technique in 2007. The reason was that the bipolar 60 Hz system frequently failed to delivery charge, and the patients were already awake for the language mapping. As the surgeon (MVCM) always asked for the NF to perform ECoG and motor mapping, the neurophysiologist (SMV) had the monopolar HF probe ready to use. Initially, we used to set THR by evoking speech arrest by counting or object naming. We used a train of 3–5 pulses of 500μS duration at 2 Hz and intensities reached up to 16 mA [59]. Currently, we set the reference electrode at the incision border, aiming to diminish facial movements (previously evoked by the reference electrode at Fz). Setting THR By HF, the stimulus THR is set (a) by evoking motor responses after direct motor cortex stimulation either with the monopolar probe (if it is exposed) or through the strip electrode (slipped over the precentral gyrus) and (b) by blocking language function in all other cases. Temporal lesions can be quite challenging to set THR. For LF protocols, cortical stimulation is started with 2 mA and may be increased up to a maximum of 6 mA or 1 mA below the intensity that evokes afterdischarges [19, 21].

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Stimulation Technique Accuracy Regarding the effectiveness of a stimulation technique, it is paramount to elicit true negatives and true positives since they determine the functional borders of the resection. A negative mapping might not be interpreted as a failure in technique accuracy if the patient presents a good postoperative neuropsychological performance [60]. Moreover, the probability of finding a positive mapping in a presumed positive region is about 40% using DES [61]. In our cohort of 41 patients using HF technique, 19 mapped negative and 22 mapped positive for language function. Immediate postoperative status indicated that nine patients who mapped positive were worse. Hence, intraoperative positivity truly identified eloquent areas, leading to transient worsening due to manipulation. Yet, in 30th-day follow-up, only 1 patient out of those 22 remained worse than before the surgery [59]. Among those patients who mapped negative, only two had immediate transient deterioration, meaning that true negatives were safely identified and the corresponding areas resected without causing functional damage. In our experience, HF language mapping has been effective for all lobes tested, with equivalent amounts of positive and negative mapping results [59]. Accordinlgy, Riva et al. [20], successfully performed HF language mapping in temporal and frontal lobes. LF and HF Effectiveness Yet, we should ask ourselves if HF is equivalent to LF for language and cognitive mapping. Riva et al. [20], gave us a glance to this matter as they compared both techniques in the same patient. Mapping results (articulatory, anomia, paraphasia) did not differ between the two stimulation methods. LF bipolar stimulation sensitivity and precision (0.458 and 0.665, respectively) were slighter higher than the HF counterparts (0.367 and 0.582, respectively). HF at a frequency of 3 Hz was less epileptogenic and resulted in speech arrest in all patients. LF was ineffective in some patients even at 12 mA. In general, double the intensity was needed by HF compared to LF to evoke language block. The major conclusions were that (1) HF could identify essential subcortical tract as efficiently as LF; (2) there was no significant difference regarding the extent of resection and functional outcome; (3) HF can be an alternative for patients with higher risk of seizures; (4) both assemblies were effective for tumors with sharper borders, less edema, and no seizure history; and (5) HF was better in cases of significant edema, infiltrative borders, and ictus clinical presentation. Later, HF has been shown to be as efficient as LF for DES during right frontal lobe mapping using the Stroop test [60, 62].

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This suggests that it may be advantageous to combine LF and HF to increase the accuracy and confidence in the mapping results [20, 43, 59]. Monopolar Versus Bipolar Probe It is not the scope of this chapter to detail probe types. Yet, we will discuss some aspects related to language protocols. For general information on bipolar and monopolar probes, refer to Chap. 11. J.B. Ranck [56], studied the effect of monopolar stimulation of intracranial myelinated white matter [56]. The current necessary to stimulate an axon is inversely proportional to its conduction velocity. This variability was a matter of fiber size and distance to the nearest Ranvier node. Fiber conduction velocities should be taken into account as a source of variation in the current-distance propagation relation. This concept applies for both monopolar and bipolar probes. Using 25 μA at 60 Hz stimulation reached up to 25 μM at lateral hypothalamus [56]. On the other hand, a monopolar cathode delivering 200 μA with a pulse of 200μS stimulated fibers of rubrospinal tract 1–1.5 mm away [63, 64]. This data is important to substantiate spatial accuracy. Yet, faster fibers in underneath the monopolar cathodal tip could eventually not be stimulated, while cell bodies and slower fibers within the radius scope of stimulus propagation would be [56]. This phenomenon is due to anodal surround. Similarly, when using a bipolar probe in the same orientation as the fiber, the cathode will depolarize and the anode hyperpolarize, resulting in the propagation of the action potential in only one direction [56]. Hence, the orientation of the bipolar a

b + 5 mm

+ -

-

Fig. 17.7 (a) By bipolar stimulation: current flows between the tips. Optimal tips distance is 5 mm allowing an optimal focusing of the charge. By cortical stimulation, current reaches cell bodies transversally. By subcortical stimulation, the orientation should be longitudinal to the fiber and current flows in direction to cathode. (b) Monopolar cortical stimulation generates a radius spread with current entering through dendrites, which are hyperpolarized and leaving through axons. The current is stronger near the tip and diminishes into reference electrode direction. Subcortical stimulation depolarizes the axon transversally and current flows into upward and downward directions

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probe is of importance to ensure successful stimulation. Although [50], reported that ideally a bipolar probe transversely activate axons, in fact, it would take four to five times more current than if placed longitudinally [56, 65]. Figure 17.7 summarizes stimulus propagation in relation to probe and neural structure. Given the same stimulus intensity, monopolar stimulation provides a radius scope of propagation, with intensity density greater surrounding the active electrode. In opposition, in bipolar probe, the electrical field lies between the round tips [19, 46, 47, 50, 66]. The optimal distance between tips for bipolar probe is 5 mm due to better focusing the current density [50]. Usually, using a monopolar probe, the anode needs twofold less charge to stimulate the cortex than the cathode, being the situation exactly the opposite regarding the axon [20, 47, 51, 56, 66]. Due to the need of triggering the language and cognitive tasks, usage of continuous subcortical mapping using a suction stimulator or even the monopolar probe is not indicated. Microdissection using these devices combined with continuous subcortical mapping is reliable only for motor pathways. For language mapping, it is mandatory to hold still the mono−/bipolar probe for 3–5 seconds during the processing of language task. It is not possible to perform language mapping while moving the device along the direction of the axon fiber. Indeed, false negatives may result from this erroneous technique application. In fact, stimulation lasts too short and there is no task triggering. Additionally, usage of bipolar coagulator and CUSA while testing can mimic the effect of stimulation and should be avoided [47].

Triggering Language and Cognitive Tasks The language stimulation is applied for 3 to 5 seconds and must be triggered by the beginning of the language task and an introductory sentence [21, 47, 48]. The most common is the ON test, in which the beginning of the question “What is this?” Table 17.1  Setup of task and mapping triggering Task Object naming

Semantic: Combination of figuresa Word repetition Spelling

Question and stimulation starts in bold What is this?

Possible findings Speech arrest, aphasia, anomia, hesitation, semantic and phonemic paraphasia, perseveration, reverberation Combine the upper figure with one Phonemic or semantic paraphasia, of the below ones hesitation Unable to matcha Repeat these three words: Unable to repeat, dyslalia, semantic Boat – Snake – banana and phonemic paraphasia Spell the following word: Incorrect or unable to spell; dyslalia Crocodile (continued)

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Table 17.1 (continued) Task Working memory

Visual memory

Short-term verbal memory

Long-term verbal memory Attention

Drawing Writing Reading Reading Color identification

Visual field Calculation

Question and stimulation starts in bold Repeat this sequence in opposite order: V4Y8M2 (e.g., letter and numbers) Crocodile – Instance – Furniture (or a set of three words) Pay attention at the following image. Remember it. I will ask you about it soon: (image of a door, e.g.) ----- ON two times ----- then back to visual memory: Which object do you remember? Pay attention at these three words that I will ask you to repeat soon: Boat – Snake – banana ----- object naming two times ----then back to verbal memory: Which words do you remember? Relate three objects/animals that start with letter M Stroop test: What is the color of the letter? (A) Interference test: What is written here? (B) Draw a fish Write the word “shark” Read the following sentence Stroop test: Option 1: What is the color of the letter? Option 2: What color is written here? Look straight at the red point. What do you see at the corners? How much is 4 times 5?

Possible findings Unable to remember one or more inputs

Unable to remember one or more inputs

Unable to remember one or more inputs

Unable to remember one or more inputs Interference:  Read the word (A).  Name the color (B). No drawing Unable to write Unable to read, dyslalia Interference:  Read the word.  Name the color.

Unable to see quadrants Unable to calculate or wrong results

Semantic can be tested even if the patient is unable to name. In this case, the patient points to the matching figure

a

corresponds to the time to start the stimulation of the mapped area (Video 17.1). We suggest a triggering chart according to different tests in Table 17.1 and Fig. 17.8. There is no consensus about prolongating the stimulation for 6 or more seconds for more complex tasks. Children pose a challenge due to CNS maturation and neuroplasticity. Longer stimulation up to 10s may be required in children or while testing negative motor area [21]. Jayakar [67], suggested that children need longer than 5 s stimulation for

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Fig. 17.8  Triggering. Presentation of language tasks and their correct trigger moment. Ray indicates temporal onset of stimulation. The 4-second stimulation began with the word “what” during the VMLA-ON task. For other tasks, stimulation lasts 5 seconds. Presentation of object lasts until the end of the retrieval period

more complex language and praxis tasks. Usually, THR for eliciting clinical response or afterdischarges is also higher in children [67]. For setting stimulus THR, ON and counting are the commonly used tests [19]. Counting could be an automatized task, limiting its accuracy. Reading aloud can be an alternative for Broca’s and Wernicke’s areas and temporal lobe [21]. Morshed et al. [19], arouse new considerations on methodological application itself. Regarding stimulus intensity, it may affect mapping results, i.e., when the current is increased, there could be a change on the type of language error, from anomia to speech arrest, for example. Additionally, it could increase the number of positive mapped points. Similarly, stimulation onset is not extensively studied. It is assumed that stimulation starts 1.4 s prior to visual presentation in order to disrupt the focal neural processing required for the motor planning of speech production. But will there be a gain if stimulation was applied through presentation response or only at the responsive phase? Moreover, how long should the stimulation last in more complex tasks? Is the 4 seconds stimulation used to ON effective for the memory task as described by Ojemann (see below)? Ojemann, 1986, reported a short-term memory test during left temporal lobectomy, aiming to spare the hippocampus: object was exposed for 4 s – a distractor for 8–12 s – and the patient had a retrieval time lasting 4 s. Stimulation occurred in any of the phases of the test. Some patients found this task difficult, and errors were frequent regardless of the moment of stimulation. Each figure took 18 to 20 seconds

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to be tested, which was too long for the intraoperative context. Consequently, only six trials were performed in patients presenting high risk for memory deficits. This report points to some questions: Is a difficult task the proper way of testing in the intraoperative environment? By memory task, at which moment should the stimulus (focal blockage) be applied? During the presentation of objects (neural processing) or by the retrieval? Potentially, prolongating the stimulus application through both presentation and response at any given language task could impact the effectiveness and sensitivity of the findings [19]. Lastly, patient should not be informed neither when he is being stimulated nor mistaken. We use team codes during testing, in which “excellent, very good” means correct answers, while errors are signalized as “positive.” Doing so, we avoid patient anxiety because of being mistaken. It is important to continuously encourage the patient with positive remarks, as “you are helping a lot” and “you are doing fine,” during the awake phase. It hinders stress and empowers the patient.

Risks Of upmost importance is that DES is safe for brain parenchyma [27, 42, 46]. For safety considerations, the maximum stimulation intensity should not exceed 40 μC/ cm2/phase when applying continuous stimulation, and by HF, it is commonly limited to 25 mA [42, 47, 49, 50]. When discussing electrical safety, several factors must be considered: charge per pulse and per train, frequency, number of pulses, total train density, and charge [43, 49, 68]. As the charge is dependent on pulse duration, the charge applied using a biphasic pulse is twice that applied using the same current but with a monophasic pulse [19, 47]. By HF, the current intensity is higher but applied for a shorter time, with less pulses per train and thus delivering less charge to the brain [20, 49]. Hence, by LF, there is a sequence of 50–60 biphasic pulses per second, summing 200–240 pulses in 4 s stimulation, and the total charge is higher. Figures  17.9 and 17.10 detail this subject and compare safety issues between LF and HF. The most common side effects of brain stimulation are afterdischarges and seizures (Fig.  17.11). Sick tissue has aberrant excitability and lower THR for ictal events [20, 42, 46]. ECoG is mandatory and allows the identification of afterdischarge THR, which should not be exceeded [19, 21, 46]. Intraoperative stimulation-­ induced seizure rate ranges from 2% to 67% particularly in patients with a previous history of seizures [17, 19, 20, 43, 59]. Riva et al. [20], in regard to HF described an incidence of epileptogenic activity of 11.9%, while we reported an incidence of 7.3% [59]. HF motor mapping poses a lower epileptogenic risk of approximately 1%, despite the higher stimulus intensity [68–70]. Epileptic events and afterdischarges are mostly elicited by longer pulses of 0.5–10 ms, perhaps due to current flow through cell bodies or dendrites [56]. Additionally, afterdischarges can simulate the stimulation effect and prevent mapping [20, 21, 43, 71]. Adding ECoG greatly enhances its identification and early

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Fig. 17.9  LF and HF train of stimulus. By LF, each pulse is biphasic, and there are 50–60 pulses per second, summing 200–240 pulses in 4 s mapping. By HF, there is a train of 4–5 monophasic pulses, resulting in 4 pulses (at 1 Hz) to 15 pulses (at 3 Hz) per second, summing 16 to 60 pulses in 4 s mapping. Pulse duration is half for HF, and there is an ISI between pulses. Consequently, resulting total charge is lower for HF

b

Series (Ref. no.)

Type of Stimulating Pulse

Charge Number of Density Charge Contact FrePulses per Duration per Pulse Intensity Surface quency Necessary Pulse (ms) ( C/ (mA) (cm2) (Hz) for One phase) ( C/ phase/ Response cm2)

Total Charge per Train ( C)

Total Charge Density per Train ( C/cm2)

King and Schell, Bipolar mono1987 (16) phasic

3–10

1.0

0.01c

50

250-500

3-10

300-1,000

750-5,000

75,000– 500,000

Ebeling et al., 1989 (9)

Bipolar monophasic

10–40

0.2

0.01c

50

>300d

2-8

200-800

>600

>60,000

Berger et al., 1990 (5)

Bipolar biphasic

16

1.25e

0.01

60

240

10

1,000

2,400

240,000

 12 μ compatible with motor fibers. These fibers would innervate the levator anguli oris muscle. Interestingly, previous report by Youssef & Downes [91], had found IN to have the amount of 3000 myelinated fibers with a diameter of 9 μ [5, 91]. Additionally, Youssef & Downes [91], confirmed previous publications from other authors and reported FN to have 10,000 to 11,000 myelinated fibers much thicker than IN. Moreover, they reported differences in amounts of myelinated fibers depending on the FN segment. In tympanic segment, they found 1,800 more fibers than in cisternal segment. Rhoton et al. [68], had described that the IN can be composed of two or more filaments, more easily identified when they joined the FN motor fibers.

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Yet, Prell et al. [62], attributed to around 150 IN motor fibers (0.5% of 3,000) the origin of confounding A-trains in perioral muscles. Although these A-trains had little clinical relevance, they stated these A-trains represented a confounding factor, interfering with correct frEMG interpretation [62]. The proposal that needles placed in the orbicularis oris or mentalis would register A-trains in the neighboring levator anguli oris requires further evidence. It should be taken into consideration Youssef & Downes and Rhoton et  al. findings  to  explain  how  A-trains are more easily evoked while manipulating intra-meatal FN segment, (where the FN lies just by the neighboring IN).

Corticonuclear Motor Evoked Potentials (CoMEP) Choosing Between Different Assemblies CoMEP aims to activate the corticonuclear motor pathway rostrally to the site of the lesion and microsurgical manipulation. It enables monitoring of FN and lower CNs (IX to XII) before their visualization and throughout the surgical procedure [1, 3, 17, 20, 84, 85]. Nerves III, IV, and VI are not amenable to transcranial electrical stimulation (TES) [10]. Yet, CoMEP is the most complex among all MEPs [20]. Anatomical peculiarities influence the results. The CN nuclei may have unilateral or bilateral afferents; muscles are small and overlapped or close to muscles receiving different innervation. Additionally, the proximity of the nuclei to the stimulus source leads to big artifacts [20, 26]. CoMEP was described during TIVA anesthesia, using mainly propofol and opioids. Described alert criteria may differ during inhalational regime, so it is strictly not recommended. Akagami et al. [3] and Dong et al. [17] (from the same group), reported successful CoMEP from VII to XII muscles after contralateral TES. The former used electrodes placed at C3/C4 to Cz and the latter used  M3/M4 to Cz (anode-cathode). Although it could be possible to produce CN-CMUAP using interhemispheric C1–C2 or C3–C4, it usually resulted in a high rate of technical failure, overwhelming stimulus artifact and patient disturbing movements [1, 3, 17, 84, 85]. Execution of double train (multipulse + single pulse) is paramount and excludes peripheral CN activation [3, 10, 15, 17]. The explanation is that corticonuclear neurons depend on temporal summation of descending volleys to be activated [10, 13]. By double-train technique, the inter-train interval is set at 70–80 ms, and total sweep is usually kept at 100 ms, so that delayed peripheral CN latencies can be identified. Healthy ipsilateral FN peripheral latency is 5 ms [3, 82] and by intracranial proximal stimulation is about 6–7 ms [17, 35, 82]. It differs from the latency of corticonuclear CMUAP, which is above 10  ms. Double train should be carried out throughout the IOM. Verst et al. [85], proposed C5/C6 to Cz (Table 19.4). Due to greater facial motor cortex proximity, it usually needs half the intensity used with C3/C4-Cz and results in less neck movements [20, 31, 84, 85]. Consequently, C5/C6 to Cz usually allows

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Table 19.4  CoMEP: assemblies and results

Authors, year Akagami et al. [3]a

Montage (anode to cathode)/ success rate C3/C4 to Cz 88%

Dong et al. [17]a

M3/M4 to Mz 92.1%

Acioly et al. C3/C4 to Cz [1]a 85–86.7%

Verst et al. [85, 86]a

C3/C4 to Cz 82.6% C5/C6 to Cz 86.9%

Rufina’s experience

M3 or M4 + 1 cm lateral to Cz

Deletis group

C3/C4 to Cz

Karakis and Simon [31]

C3/C4 + 2 cm lateral and inferior to Cz

Hiruta et al. [26]

C3/C4 to Cz 84.9%

Technique To3 to To5 ISI 1–3 ms Pulse duration: 50uV To3 to To4, ISI 2 ms Pulse duration: 50uS or 500 uS To3 to To5, ISI 2 ms Pulse duration: 50uS To3 or To4 ISI 2 ms Pulse duration: 500uS 0.5 to 2 Hz To3 to To4 ISI 2 ms Pulse duration: 50 to 75uS To3 to To5 ISI 2 to 4 ms Pulse duration: 500uS 2 to 3 Hz To3 to To4 ISI 2 ms Pulse duration: 500uS To5 to To8 ISI 1.4–1.6 ms Biphasic pulse 400uS Double train (ITI 50–100 ms)

Recording muscles and latency O oris 12 to 16 ms

O oris 10.9 to 15.1 ms

Sensitivity/ specificity S 90%/Sp 89%

>50% S 100% >65%: S 91%/Sp 97% a S 53.8/Sp 100%

OO: 10 to 24.5 ms O oris: 10 to 23.4 ms OO, M >50%: S >10 ms 92.8%/Sp 66% >60%: Not informed F, OO, N, O Not informed oris

CMUAP loss versus FN outcome >50%

>50%: Mild >65%: Moderate 100%: Severe >20% for OO >65% for O orisa >50% mild >65% moderate to severe

>50% mild >65% moderate to severe

OO, N, O. oris, M Vocal cord CHTY

Not informed >80%: Mild to moderate Loss: Permanent

F, OO, O oris, M

Not informed >50%

O oris Latency not informed

Recovery value 80% deterioration. Patient’s immediate HB was 4

managed to record THR-CMUAP in 90% of their sample and related an increase 50%) is observed, it is recommended to reduce the load until parameters return to baseline. The main mechanism of injury is vascular, and therefore, the alterations may not be immediate. Thus, surveillance with Tc-MEP must last at least 10 min after the traction.

Fig. 22.3  Tc-MEP responses of the left lower limb: transient amplitude drop in the femoral nerve territory. Red circle: Tc-MEP amplitude drop in the iliopsoas and quadriceps muscles; Green circle: Tc-MEP amplitude recovery after repositioning the cushions at the level of the anterosuperior iliac spines

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D. Muscle Recording Muscle recordings, mandatorily, must be done with recording and reference electrodes inserted in the SAME muscle. This information may seem obvious, but it is not uncommon to observe the so-called hybrid recording in some protocols. We emphasize that in deformity correction surgeries, the segmentation of root territories is of particular importance for accurate diagnosis, in both EMG-ST and Tc-MEP. Positioning After the patient is transferred to the ventral decubitus, the neurophysiological tests should be repeated and compared with the baselines previously recorded in dorsal decubitus. It allows technical and anesthesiologic checklist. Moreover, the baseline in dorsal decubitus can identify previous neurological deficits.

Intraoperative Deformity correction surgery has main steps, and IONM should follow each one. Therefore, a step-by-step IONM protocol is proposed below.

Step-by-Step IONM Protocol 1 . Exposure of anatomical planes – EMG-fr, Tc-MEP, and SSEP 2. Instrumentation – pedicle screws: EMG-ST, Tc-MEP, and SSEP 3. Instrumentation – sublaminar bands or hooks: EMG-fr, Tc-MEP, and SSEP 4. Osteotomies – EMG-fr, Tc-MEP, and SSEP 5. Placement of rods – Tc-MEP and SSEP 6. Deformity correction – Tc-MEP and SSEP 7. Closure by planes – Tc-MEP and SSEP Considerations • Step 1: After MEP baselines in ventral position, neuromuscular blockade with rocuronium may be done, as described under the topic 4.2. If used, Sugammadex® should be administered before the next step. • Step 2: During the pedicle screw instrumentation, there is the risk of direct lesion of the medulla (thoracic screws) or cauda equina (lumbosacral screws), in the case of medialization of the screw and rupture of the medial wall of the pedicle. Special attention should be given to the proximity of the spinal cord to the pedi-

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Fig. 22.4  MRI: Apex of the concavity curve. This shows the proximity of the spinal cord to the pedicle vertebra in the concavity of the curve

• • •

•

• •

cle vertebra in the concavity of the curve (Fig. 22.4). Additionally, the perforation and transfixation of any pedicle cortical (superior, inferior, lateral, or medial) may result in radicular lesion. Therefore, EMG-ST and Tc-MEP and SEP should be performed. During thoracic instrumentation, Tc-MEP should be performed intermittently after each pedicle instrumentation, interspersed with EMG-ST. The particularities of EMG-ST at this stage will be addressed in the topic “Transpedicular Neurophysiological Navigation” (section “Pedicle Instrumentation”). Step 3: Sublaminar bands and hooks can serve as a supporting element for the corrective rods. They can cause direct injury to the neural tissue, which can be identified by SSEP because of injury to the dorsal column of the spinal cord (Fig.  22.5). Interspersing EMG-ST with EMG-fr and Tc-MEP allows prompt identification of adverse events and reversal of the maneuver. Step 4: Osteotomies are critical steps with a high risk of spinal cord injury. Ponte’s osteotomy approach is the most used. Indeed, the greater the resection of vertebral elements in an osteotomy, the greater the exposure of the spinal cord and, consequently, the greater the risk of inadvertent percussion by the instruments. Thus, continuous monitoring with EMG-fr, Tc-MEP, and SEP is paramount. The presence of neurotonic discharges in EMG-fr is suggestive of neural insult, which is checked with Tc-MEP, and, if necessary, a pause in the maneuvers to await recovery is requested (Fig. 22.6). Usually, the direct spinal MEP (D-wave) has no indication in deformity surgeries because the instrumentation generally extends to the lumbar levels. However, our protocol includes D-wave in very particular cases, such as in acute angle congenital kyphoscoliosis involving hemivertebrae or vertebral fusions in the thoracic territory. In our experience, during the osteotomy phase at the apex of the deformity, or even during spinal decompression in cases of stenosis, D-wave

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Fig. 22.5  Tibial nerve SSEP responses during the placement of sublaminar bands in the left T8 vertebra. In the left lower limb (left responses), a transient amplitude drop was observed during this surgical step. The surgeon was alerted and stopped the maneuver; after that, the responses recovered

Fig. 22.6  Tc-MEP amplitude drop during osteotomy of right T6 level. The surgical team was alerted and the responses showed a recovery, after a brief pause of the maneuver

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may act as an additional parameter to control the integrity of the motor pathways, enabling the surgery to proceed, even if there is a drop or loss of Tc-MEP responses (Note of the editors: exclusively reflects the experience of the authors). Step 5: The rod placement step is generally harmless to neural structures. However, the exception is in the correction of kyphosis when the cantilever maneuver is applied. In this situation, correction of the curve occurs simultaneously with rod placement. Tc-MEP and SSEP tests should be performed. Step 6: Curve correction: IONM improved safety during rotation and translation of the vertebrae, allowing more aggressive corrections. Strict control with Tc-MEP and SEP must be done. Additionally, it is particularly important to control physiological anesthetic, hemodynamic, and hematimetric parameters because the greatest risk is vascular injury and spinal cord ischemia. If IONM points to neurological dysfunction, the corrective maneuver should be reversed, and a less aggressive correction should be considered. Step 7: Final neurophysiological tests.

Pedicle Instrumentation During pedicle instrumentation, EMG-ST has major importance. The goal is to map the neural structures near the instruments and screws used. The EMG-ST is performed using a monopolar stimulator probe (cathode -) and a subdermal needle electrode (anode +). The needle is inserted in the contralateral paravertebral musculature at the same level being tested. To minimize the risk of nerve injury, our protocol includes stimulating during the following steps: 1. Facet joint 2. Punctor 3. Pedicle finder 4. Pedicle tap 5. Ball tip probe 6. Screw placement 7. Pedicle screw head Performing EMG-ST at each step is important since an early detection of incorrect path allows for prompt re-evaluation of the technique. Consequently, it avoids multiple path attempts at the pedicle, which could ultimately culminate in cortical violation and/or fracture and inability to instrument the desired level. Calibrations Intensity (I)  the depolarization threshold can be determined pedicle by pedicle. We start with 7 mA for thoracic pedicles and 10 mA for lumbar pedicles, using a single pulse of 200 uS or 0.2 mS for the massif screws and 50% more intensity when the

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screws are cannulated. The intensity may be adjusted if a response is present on the facet joint, indicating the need to reduce the stimulus to adequate values. Duration (D)  the total energy charge in microcoulombs (C) is calculated by the formula:

C = I × D ( intensity × duration )



Therefore, as important as the intensity of the pulse is its duration. In our protocol, we use a duration of 200 μS or 0.2 mS. To exemplify: 10  mA  ×  100  μS: 1000  μC; 10  mA  ×  200  μS: 2000  μC; and 10 mA × 300 μS: 3000 μC. Thus, pulses of the same intensity with different duration will have very different final energy charges. We highlighted this concept because threshold vary among IONM groups and the surgical team should be aware of the concept of total load, and whenever they ask about intensity, they should also ask about duration. Using total load parameter enhances patient’s safety despite the differences between stimulation protocols. Frequency  for lumbar screws, simple pulse is used, once the structures at risk are peripheral nerves (spinal nerve roots or lumbosacral plexus). For thoracic screws, a train of pulses is used, because they facilitate the depolarization of the spinal cord, in the case of the medialization of the screw. The recommended configuration is 4 pulses of 0.2 ms duration with an interstimulus interval (ISI) of 2 ms (Calancie et al. 1990) [6, 8, 9]. Pedicle Depolarization Threshold In scoliosis, the surgeon sometimes leads with hypoplastic or even virtual pedicles, especially in the concavity of the curve [69]. In these cases, it becomes even more important to determine the pedicle depolarization threshold by stimulating the facet of the vertebra of the level being instrumented. Lumbar vertebra: start with an intensity of 10 mA and a pulse duration of 200 μs. If there is a response in the EMG-ST, the intensity of the stimulus should be progressively reduced until no more response is obtained. This value is considered the depolarization threshold of this pedicle and is used as a parameter for instrumentation. The cutoff point (lower limit) is a total charge of 1400 μC, that is, intensity of 7.0 mA. If stimulation is positive below 7 mA, which is the minimum acceptable safety value, the pedicle path is considered unproper according to the neurophysiological parameter. In this situation, the surgical team performs careful radiological control, visualization, and palpation of the pedicle to decide about redoing the path or not. Thoracic vertebra: the technique recommended by Calancie (2014) [8, 9] consists of using the four-pulse train, ISI of 2 ms, duration of 0.2 ms, frequency of 3 Hz, and intensity of 10–15 mA (screw path) – total load from 2000 to 3000 μC/pulse. However, especially in cases of children’s scoliosis and underweight adolescents, in

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which there is a higher prevalence of narrow pedicles, this proposed total load can generate false positivity. Thus, in our practice, we use all the parameters mentioned above, except for intensity; the threshold used in our protocol is 7–10  mA (total load: 1400–2000  μC/pulse), and the cutoff is 7  mA.  We recommend reading the original paper of Calancie (2014) [8, 9] for a more comprehensive understanding. (Note of the editors: exclusively reflects the experience of the authors. However, they have been performing IOM in disable children for the last 27 years). Discarding the False Negatives In the absence of a myotomal response with EMG-ST, a quick checklist should be performed to avoid false negatives. This checklist is composed of three main factors, according to their potential source of error: stimulator, patient, and screw. Regarding the stimulator: 1. Is the subdermal needle (anode) inserted into the paravertebral muscle and does it contract rhythmically? This is a practical way to check if the stimulus is being applied. 2. Is the needle/anode placed at the same level as the screw to be stimulated? It is necessary for focal stimulation and to avoid “spread.” When the anode is kept “stationary,” far from the cathode (stimulator), false results may occur, including responses in myotomes far away from the pedicle level being instrumented. 3. Is the tip of stimulator being properly applied? The shafts are covered with electrical insulation, and the surgeon should be aware of that (Fig. 22.7). 4. Is the stimulator turned on and properly charged? Always evaluate if the electrical circuit is closed. Regarding the patient: 1. Is the patient under the effect of pharmacological neuromuscular blockers? To answer this question, apply the train of four (TOF) test. Of note, the reversal of neuromuscular blockade does not occur at the same time in all four limbs after administration of the antagonist. Lower limbs may take longer to reverse neuromuscular blockade compared to upper limbs [4]. 2. Does the patient have polyneuropathy or chronic radiculopathy? In these cases, the depolarization threshold may be higher than normal [67]. Regarding the screw: 1. Is it massif or cannulated? The cannulated screw has a higher depolarization threshold. In our protocol, we increase the intensity of the stimulus by 50% compared to the massif screw, with a safety margin above what has been performed by other groups [72]. It is important to stimulate the guide wire of the cannulated screw and then the head of the screw already positioned. 2. Is the screw covered with hydroxyapatite? In this case, the inside hole of the probe should be stimulated, because the screw itself is totally isolated to the passage of electric pulses.

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Fig. 22.7  Correct use of the stimulator probe electrode. Only the tip of the probe is uncovered; the shaft is covered with electrical insulation

a

b

Fig. 22.8  Coaxial screw – head stimulation. (a) Incorrect: stimulation in the screw crown and (b) Correct: stimulation directly in the screw

3. Is the screw made of metallic materials of different conductance? The polyaxial screws, after being introduced, should be stimulated inside the crown where the screw is. The reason is that they are materials of different compositions, not maintaining perfect contact with the screw, until it is coupled to the rod and connector (Fig. 22.8).

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After the checklist, the negative response can be taken as a true negative. Yet, it may not be anatomically well positioned in the image, because it may be in the intervertebral disc space or on the side of the vertebral body, without proximity to any neural structure. Discarding the False Positives In the case where there is a response on the EMG-ST, a checklist of two factors must be performed: stimulator and patient. Regarding the stimulator Is there no coherence of the response in the EMG-ST with the instrumented level? In some cases, a more cranial response is generated at a non-adjacent level. For example, the surgeon is instrumenting the pedicle of L5, and a response is observed at L1/2. In these cases, it is important to observe if the needle (anode) is correctly placed at the same stimulated level. Regarding the patient 1. Does the patient have osteoporosis? Bone porosity can allow the stimulus to spread through the wall of the pedicle, lowering the depolarization threshold. In this case, testing the depolarization threshold of the pedicle through the facet joint is an important step. 2. Does the patient have vertebral canal or intervertebral foraminal stenosis (more frequent in adult scoliosis)? Root proximity to the cortical of the pedicle can also facilitate the “spread.” Often, in cases of stenosis, even with imaging showing adequate implant location, the EMG-ST evokes persistent responses that usually disappear after decompression  – simply because of increasing the distance between the root and the pedicle. 3. Is there a fracture in an adjacent or underlying vertebra? Some fractures in the wall of these pedicles may be imperceptible by surgical palpation or on imaging exams. This fracture may spread electrical stimulus and elicit responses on EMG-ST. 4. Is the pedicle too narrow? Sometimes the same vertebra can have pedicles of different diameters and shapes, and the depolarization threshold of each one should be determined (Fig. 22.9). After this checklist has been run out, a positive response to stimulation means the screw is “functionally” misplaced and repositioning must be considered (Fig. 22.10). Conversely, this does not mean that it will be inadequate in the image. Fluoroscopy does not have a three-dimensional image, and the parallax phenomenon can lead to misinterpretation. Despite the 3D O-ArmR facilitation of pedicle instrumentation, errors are still possible since it is a mathematical model image.

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Fig. 22.9  Pedicle assimetry in the same vertebra

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Fig. 22.10  EMG-St responses during lumbar right L5 pedicle instrumentation. (a) Presence of response in screw stimulation; (b) After screw repositioning, no response to stimulation is seem

Transpedicular Neurophysiological Navigation One of the techniques used for pedicle screw insertion is the “freehand technique” [10]. With the EMG-ST, we can perform what we call “transpedicular neurophysiologic navigation,” during the freehand technique, which is the stimulation of all steps of the pedicle instrumentation. This information is continuously communicated to the surgeon, who makes the proper correlation with the surgical step and, if necessary, performs the immediate correction of the implant trajectory (introductory probes and/or screw). Thus, deviations of the path while perforating the pedicle can be promptly identified; even at the early phase of the pedicle finder use, promoting the recognition of the direction the cortical invasion is likely to be. An additional advantage is that these steps can be performed without the concomitant use of radioscopy, which reduces operative time and exposure to radiation.

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For a better understanding of this technique, we cite some examples of its application. Transpedicular Neurophysiological Navigation: Example L4 Pedicle (Fig. 22.11) 1. Presence of responses in the myotome of L3: interpret as cranial or lateral course of the screw, since this root emerges in the immediately superior foramen and passes laterally and juxtaposed to the pedicle. 2. Presence of responses in the myotome of L4: interpret as the caudal trajectory of the screw since this root emerges from the inferior foramen to this pedicle. 3. Presence of responses in the myotome of L5 and/or multirooted: interpret as a medial route of the screw. Fig. 22.11 Transpedicular neurophysiological navigation: schematic figure of the lumbar vertebral pedicles and their correlation with the nerve roots

482 Fig. 22.12  Bicorticalization of the S1 screw. (a) Anatomical diagram demonstrating the proximity of the lumbosacral plexus in the anterior position of the S1 vertebra. (Courtesy of Moura Filho, JP and Bordalo-Rodrigues et al. 2020 [39]). (b) Bicorticalization of an S1 screw on CT

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a

b Transpedicular Neurophysiological Navigation: Other Examples 1. Multi-radicular responses: these responses are usually present when there is medialization of the screw, in both the lumbar and thoracic pedicles. 2. Pedicle of S1: when there is bicorticalization of the screw, EMG-ST may show responses in the L5 root or in multiple root levels, due to the anatomical disposition of the roots and lumbosacral plexus in the anterior portion of this vertebra (Fig. 22.12).

Decision-Making Algorithm Based on Alarm Signals The prompt identification of a potential neural insult and its cause leads the surgical team to react to avoid tissue injury and its sequelae (definitive or transitory) if the maneuver allows reversibility. Thus, a management algorithm should be established and followed when facing alarm signals. The importance of checklists in times of stress in the operating room has been developed and suggests a decrease in the incidence of errors [75]. In addition to the detection of real events (true positives), it is part of the skills of the neurophysiologist to minimize the false-positive rate as much as possible, thus improving the positive predictive value of the test. A false-positive event generates unnecessary

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interruption, increases the stress of the surgical team, and brings IONM into discredit. Although there are alarm criteria recommended for each test (EMG-fr, SSEP, and Tc-MEP), the algorithm is exclusively based on alterations of Tc-MEP.  The reason is that MEP is more susceptible to ischemia, being the one that changes the earliest in cases of spinal cord injury [55]. Additionally, MEP is the first to return to basal levels after the appropriate interventions are made. Alarm Signals: Tc-MEP Alarm parameters diverge in the literature [7, 28–30, 32, 48, 53, 54, 56, 60, 70, 76]. The main ones are summarized in Table 22.2. In daily practice, these parameters are valued with caution (Fig. 22.13). Indeed, a reduction in the number of phases and a 50% drop in the amplitude of responses should be correlated to the moment of the surgery and precipitate exclusion of confounding factors (neurophysiological and anesthesiologic checklist). In deformity surgeries, drops of up to 80% of the Tc-MEP can be tolerated [30]. Table 22.2  Mostly recommended Tc-MEP alarm signals Alarm criteria Analysis Major “All or nothing” Minor/ Amplitude moderate Threshold Morphology Mixed index

a

Author Kothbauer et al. [28]

Characteristic Presence or absence of response

Langeloo et al. [30]

Reduction – amplitude of responses (80%) Increase in response strength at 100 V Reduction in the number of phases

Calancie et al. [7] Quinones-Hinojosa et al. [54] Segura et al. [56]

b

Index of latency, amplitude, duration, and area

c

d

Fig. 22.13  Examples of deterioration of Tc-MEP responses. (a) Normal response; (b) Reduction in the number of Tc-MEP phases; (c) Decrease in amplitude; (d) Absence of responses; (Images: courtesy of Maria Lúcia Mendonça, MD)

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Based on these algorithms and guidelines, and our clinical experience, we developed our protocol [20]. Alarm signal: Tc-MEP amplitude drop >50% – decision-making Perform neurophysiological and anesthesiologic checklist before alerting the surgical team: • Neurophysiological checklist: check the condition and impedance of recording and stimulator electrodes, output current, amplifier setup input, and stimulation parameters. • Anesthesiology checklist: check on which drugs are being used (attention to inhalation anesthetics), their doses, and if a bolus has been administered. It is important to pay attention to the level of hypnosis through the BIS, which should be >45, MAP >85 mmHg, temperature > 36.0 °C, and HB > 10 g/dl. After performing these checklists, any mistakes were found? • NO, no mistakes were noted on the checklists: this is a true positive; the surgeon will be communicated. • YES, there was an error in the checklists: make the appropriate correction of the inadequate parameter. Once the appropriate correction of the anesthesiological or neurophysiological factors has been made, have the responses returned to the previous parameters? • YES, the responses return to previous parameters: considered false positive, it is not necessary to communicate the surgical team. The surgery may continue. • NO, the responses remain altered, maintaining the amplitude drop: considered true positive, the surgeon should be notified. Communicating a true positive The surgeon evaluates if there is a cause-and-effect correlation between the reported alarm signal and the surgical time: • YES, there is a cause-and-effect correlation: the surgeon reviews only the last surgical step. • NO, there is no cause-and-effect correlation: probably, these findings may be “late changes” related with earlier surgical steps, which should be reviewed. Does the maneuver allow reversibility? • NO, this event does not allow reversibility: it is recommended to interrupt the surgical procedure and wait until the return of acceptable responses in the tests. • YES, this event allows reversibility: the surgeon will take appropriate actions and observe if IONM signals recover.

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Did the result of the reversibility maneuver or the waiting period led to recovery of the responses? • YES, there was recovery between 40% and 60% of the values from the last baseline, updated immediately after these maneuvers: continue the surgery. • YES, however, with poor recovery of responses (less than 40%) after all facilitating maneuvers (MAP increase, hypnosis with BIS >45, temperature > 36 °C, and Hb >10 g/dL): perform the wake-up test. Depending on the surgery, the hypothesis of suspending the surgery should be considered, with a second approach later to finish the procedure. • NO, the responses do not recover, are still below 20%, or are absent: perform the wake-up test. Wake-up test: voluntary and active movement of the lower limbs was observed? • YES, the patient presents voluntary and active movement in the lower limbs: continue the surgery. • NO, the patient does not present voluntary and active movement of the lower limbs, and it proves the findings of the IONM: the correct conduct is the immediate suspension of the surgery, with removal of all implant materials. In cases of wide osteotomies, the maintenance of some support rod can be considered. Note: while waiting for the patient to wake up, Tc-MEP continues to be performed. If acceptable Tc-MEP responses (up to 40–60% reduction from baseline) recover within this period, due to simple suspension of anesthetic drugs and reduction of hypnosis, the wake-up test can be canceled, and surgery continued. Postoperative Guidance and Clinical Monitoring During postoperative care after surgery for deformity correction, it is advisable to refer the patient to the ICU and maintain MAP above 85 mmHg and Hb > 10 g/dL, mainly in the first 48 h. Also, it is recommended to perform a basic neurological examination to check active movement of the lower limbs, every hour. Careful motor evaluation is important, as it can diagnose the occurrence of late neurological deficits, secondary to hematoma formation, implant displacement, or even bone spicules due to intracanal or foraminal osteotomies. False Positives and False Negatives False positives or negatives in IONM should be analyzed in relation to the neural pathway versus test performed. In older reports, SSEP was the only test performed during spinal deformity surgeries. Therefore, SSEP changes were erroneously correlated to the postoperative motor status [35]. Careful methodological analysis should always be done because conclusions could have originated from mistaken assumptions. Of note, SSEP assesses the proprioceptive pathways of the dorsal column of the spinal cord, and Tc-MEP assesses the motor pathways of the spinal cord.

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False-negative SSEP can only be so-called if no change in the sensory potentials was recorded and there is a clinically detectable postoperative proprioception deficit. False-positive SSEP, on the other hand, occurs if significant and persistent changes in SSEP are registered but with no postoperative proprioception impairment. Statements about motor impairment based solely on SSEP are inaccurate. Tc-MEP checks on motor pathway and should be performed throughout the surgery. Lastly, sensibility impairment of the lower limbs results in gait disability justifying the absolute necessity of SSEP in the spinal approaches. Thus, the tendency to use only Tc-MEP to the detriment of SSEP is a mistake: both must be used concomitantly. Usually, the term true positive is used to describe an abnormality in IONM followed by a new deficit. However, such nomenclature is misleading in terms of evaluating the performance of IONM. The purpose of the IONM is not simply to predict postoperative neurological status, but rather to alert the surgical team of possible neurological damaging events during a particular maneuver, in time to avoid the injury. Neurophysiological changes, when detected, allow a revision of the procedure by the surgeon to completely reverse or at least reduce the severity of the lesion. Therefore, when transient alteration occurs in IONM and technical/anesthetic/systemic reasons have been excluded, it means that this patient had a real (true positive) but reversible neurophysiological dysfunction, having a positive result during IONM but no postoperative neurological deficit at the outcome. This finding is commonly, but mistakenly, called false positive, suggesting that abnormal IONM signals during the intraoperative period occurred but without actual neurological injury at the outcome. Yet, they should be considered as true positives, even if they have been correctly reversed by surgical team, either by interrupting the adopted maneuver or by reversing it. Based on these facts, we disagree that the IONM has its importance or “evidence” only related to the “outcome.” The correct intervention of the surgical team facing the neurophysiological alarms allows the performance of reversing maneuvers. Thus, it prevents neurological injury and reverses a true positive to normality, modifying the outcome.

Evidence Level IONM has been used in spinal deformity surgery since the 1970s [41]. Early descriptions consisted of technical notes, case reports, and case series using SSEP. Nuwer and Cols (1995) [44] conducted a pioneering study with surgeons from the Scoliosis Research Society (SRS) and the European Spine Deformity Society (ESDS), evaluating the role of SSEPs in spine surgeries, and concluded that there had been a significant reduction of neurological lesions. However, the number of false-negative cases was still great. Indeed, it could have been expected since SSEP evaluates solely the sensory pathways of the posterior horn of the spinal cord and cannot predict lesions in the corticospinal tracts. After the association of MEPs in spinal

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surgery, subsequent studies demonstrated greater sensitivity and specificity in detecting lesions in the motor pathway [36, 37, 62]. Systematic reviews have demonstrated the role of multimodal IONM in spinal deformity surgeries [63, 65]. Fehlings et al. [16] performed a meta-analysis of 32 studies (out of 103 evaluated) and concluded that there is strong evidence that IONM is sensitive and specific in detecting intraoperative neurological lesions, and its use is recommended in spine surgeries where there is a risk of spinal cord or radicular injury. Thirumala et al. [63] evaluated 3284 patients with idiopathic scoliosis, submitted to surgical correction, showing that IONM had a sensitivity of 76.5% and specificity of 95.1% in detecting neurological lesions. Patients who had a new deficit postoperatively were 79.4 times more likely to have had significant changes in SSEP and/or MEP during corrective procedures. Other studies with large cohorts of patients have shown similar results, but all showing very high sensitivity (99.6–100%) and specificity (91.5–99.3%) [50, 52, 55, 64, 65]. These results show that IONM is very sensitive in detecting new deficits and the occurrence of falsenegative cases (presence of neurological lesion with normal IONM) is very rare. The slightly lower specificity means that an IONM change does not result in neurological deficits (false positive) but has originated from external factors like use of muscle relaxants, volatile anesthetics, dexmedetomidine, clonidine, hypovolemia, hypotension, hypothermia, and finally technical problems. In addition to detecting impending neurological damage, IONM has been shown to provide surgeons with real-time information needed to make intraoperative decisions that preserve neural function. Schwartz et al. [55], in a multicenter study evaluating 1121 patients operated on for adolescent idiopathic scoliosis, showed a postoperative neurological deficit rate of 0.8%. Thirty-eight patients (3.4%) had significant changes in IONM (SSEP and/or MEP), and of those, 29 (2.6% of the total) were attributed to specific intraoperative maneuvers (mostly by application of corrective forces and by clamping of segmental vessels). Of these patients who had a drop in evoked potentials, 88% responded to the measures adopted by the surgical team, with improved responses. This favorable result was due to the rapid response to the changes observed in the IONM, being responsible for the decrease in the presence of neurological deficit in 1.2% of all patients. In a study evaluating patients undergoing high-risk deformity surgery requiring three-spine osteotomy (osteotomy with pedicle subtraction, spine resection, and partial spine resection), Jarvis et al. [25] described that the adoption of corrective measures in cases where there were significant changes in the IONM led to a 14% reduction in postoperative neurological deficits, which recovered in approximately 1 month, with no permanent lesions observed. Other studies were also conclusive in demonstrating the facilitating role of early and effective IONM interventions [22, 36, 50]. To avoid permanent neurological damage and rule out false-positive cases as much as possible, studies have been conducted with algorithm and checklists to be followed in cases in which there are significant changes in the IONM. Vitale et al. [70] published guidelines based on a consensus of 21 surgeons specialized in spinal deformities in adults and children and on previous SRS and American Association of Neuromuscular and Electrodiagnostic Medicine (AANEM) guidelines. These

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guidelines have served as a model for several algorithm published in subsequent years and for use in daily practice. Other recent studies with large numbers of patients with spinal deformities have also suggested similar algorithms [5, 65]. The common principles among these guidelines are good communication between the surgical team (comprising the surgeon, anesthesiologist, and clinical neurophysiologist), confirmation that real alarm events exist (with the exclusion of systemic and technical confounders), consideration of performing the Stagnara wake-up test, and taking effective intraoperative measures to reverse the observed warning signs and preserve neurological function. Our algorithm, presented earlier in this chapter, follows these general principles, coupled with our clinical experience [18]. In addition to the risks from maneuvers with corrective forces (distraction, contraction, and rotation) and osteotomies, there is a considerable risk of myelopathy in instrumentation of pedicle screws in the thoracic spine. Calancie et al. [8, 9] published, in two parts, an elegant study in which they demonstrated the importance of EMG-ST in detecting medial malposition of pedicle screws in the thoracic spine. It was the first blinded and randomized study to implement a new IONM technique that, besides identifying a clinically relevant alteration with high sensitivity, also proved to be effective in providing actions to reverse the problems identified. Surgeries to correct spinal deformities are the procedures in which the role of the IONM has been studied the most. They also have the strongest evidence and recommendations. The latest SRS statement states that in surgery for spinal deformities, “intraoperative neurophysiological monitoring of the spinal cord is no longer investigational (as it was defined in the last consensus of 2009), but rather a ‘standard of care’ modality when there is a risk of spinal cord injury” [22]. Numerous studies have conclusively demonstrated that IONM is important in detecting impending spinal cord injury and facilitates early interventions for the purpose of functional preservation [11–13, 31, 40, 43, 46, 54, 58].

Conclusion Even in the hands of the most experienced and skilled surgeons, scoliosis correction surgery carries risk to the neural structures. The main critical steps from a neurological point of view are instrumentation with pedicle screws, pedicle, or facet hooks, sublaminar bands or wires, osteotomies, and the correction of the deformity. There is a triad in the operating room, surgeon, anesthesiologist, and neurophysiologist, and the communication between them should be continuous and fluent. This interaction avoids false results and neural lesion. The anesthesiologist is responsible for meticulous control of the hemodynamic and physiological parameters, ensuring adequate spinal cord perfusion, and avoiding clinical fluctuations. The neurophysiologist is not a passive observer of signals on a screen but rather an active team member. He should provide IONM as an useful tool for the surgeon

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and anesthesiologist. By understanding about spinal pathologies and surgical techniques, he helps the surgeon step by step in what we call neurophysiological navigation. Additionally, this interaction avoids false positives and negatives. Finally, IONM has gained importance in deformity surgery due to the evolution of the surgical approach itself. It is now possible to perform pedicle instrumentation, osteotomies, and correction of vertebral rotation and translation in a single surgical procedure.

References 1. Anschel DJ, Aherne A, Soto RG, Carrion W, Hoegerl C, Nori P, et al. Successful intraoperative spinal cord monitoring during scoliosis surgery using a total intravenous anesthetic regimen including dexmedetomidine. J Clin Neurophysiol. 2008;25(56):61–6. 2. Bala E, Sessler DI, Nair DR, McLain R, Dalton JE, Farag E, et al. Motor and somatosensory evoked potentials are well maintained in patients given dexmedetomidine during spine surgery. Anesthesiology. 2008;109:417–25. 3. Batko I, Koœcielniak-Merak B., Tomasik, P.J. et al. Lidocaine as an element of multimodal analgesic therapy in major spine surgical procedures in children: a prospective, randomized, double-blind study. Pharmacol. 2020;72:744–55. https://doi.org/10.1007/s43440-020-00100-7. 4. Betz M, Aguirre J, Schubert M, Götschi T, Huber B, Schüpbach R, et al. Hand or foot train-­ of-­four tests and surgical site muscle relaxation assessed with multiple motor evoked potentials: a prospective observational study. Eur J Anaesthesiol. 2020;38(8):872–9. https://doi. org/10.1097/EJA.0000000000001398. PMID: 33259448. 5. Bjerke BT, Zuchelli DM, Nemani VM, Emerson RG, Kim HJ, Boachie-Adjei O. Prognosis of significant intraoperative neurophysiologic monitoring events in severe spinal deformity surgery. Spine Deform. 2017;5(2):117–23. 6. Calancie B, Lebwohl N, Madsen P, Klose KJ. Intraoperative evoked EMG monitoring in an animal model. Spine. 1992;17(10):1229–35. 7. Calancie B, Harris W, Broton JG, et  al. “Threshold-level” multipulse transcranial electrical stimulation of motor cortex for intraoperative monitoring of spinal motor tracts: description of method and comparison to somatosensory evoked potential monitoring. J Neurosurg. 1998;88:457–70. 8. Calancie B, Donohue ML, Harris CB, Canute GW, Singla A, Wilcoxen KG, et  al. Neuromonitoring with pulse-train stimulation for implantation of thoracic pedicle screws: a blinded and randomized clinical study. Part 1. Methods and alarm criteria. J Neurosurg Spine. 2014;20(6):675–91. PMID: 24684171. [cited 2014 Apr 1]. Available from https://doi.org/1 0.3171/2014.2.SPINE13648. 9. Calancie B, Donohue ML, Moquin RR.  Neuromonitoring with pulse-train stimulation for implantation of thoracic pedicle screws: a blinded and randomized clinical study. Part 2. The role of feedback. J Neurosurg Spine. 2014;20(6):692–704. PMID: 24684176. [cited 2014 Apr 1]. Available from: https://doi.org/10.3171/2014.2.SPINE13649. 10. Cavali PTM, Kelft EV, editors. Surgery of the spine and spinal cord. A neurosurgical approach. Springer; 2016. p. 263–79. Available from: https://doi.org/10.1007/978-­3-­319-­27613-­7_17. 11. Chang SH, Park YG, Kim DH, Yoon SY.  Monitoring of motor and somatosensory evoked potentials during spine surgery: intraoperative changes and postoperative outcomes. Ann Rehabil Med. 2016;40(3):470–80. 12. Chen J, Yang J, Deng Y, Shao XX, Huang ZF, Yang JL. A retrospective study of surgical correction for spinal deformity with and without osteotomy to compare outcome using intraoperative neurophysiological monitoring with evoked potentials. Med Sci Monit. 2020;26:925371.

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13. Cho SK, Lenke LG, Bolon SM, Pahys JM, Cho W, Kang MM, et al. Can intraoperative spinal cord monitoring reliably help prevent paraplegia during posterior vertebral column resection surgery? Spine Deform. 2015;3(1):73–81. 14. De Kock M. Expanding our horizons: transition of acute postoperative pain to persistent pain and establishment of chronic postsurgical pain services. Anesthesiology. 2009;111(3):461–3. 15. Engler GL, Spielholz NL, Gernhard WN, Danziger F, Merkin H, Wolff T.  Somatosensory evoked potentials during Harrington instrumentation for scoliosis. J Bone Joint Surg. 1978;60:528–32. 16. Fehlings MG, Brodke DS, Norvell DC, Dettori JR. The evidence for intraoperative neurophysiological monitoring in spine surgery: does it make a difference? Spine. 2010;35(9):37–46. PMID: 20407350. [cited 2010 Apr 20]. Available from: https://doi.org/10.1097/ BRS.0b013e3181d8338e. 17. Feng F, Tan H, Li X, Chen C, Li Z, Zhang J, et al. Radiographic characteristics in congenital scoliosis associated with split cord malformation: a retrospective study of 266 surgical cases. BMC Musculoskelet Disord. 2017;18(1):420. PMID: 29058584. Available from: https://doi. org/10.1186/s12891-­017-­1782-­z. 18. Ferreira RJR. Neurofisiologia intraoperatória. In: Pudles E, Delfino HLA, editors. A coluna vertebral – conceitos básicos. Soc Bras de Coluna. Artmed; 2012. p. 85–94. Portuguese. 19. Ferreira RJR. EMG stimulated in pedicle screw instrumentation using the free hand technique: how to avoid common errors and rule out false results. Braz Spine Soc Newsl. 2018;18:18–9. 20. Ferreira RJR, Segura MJ. A proposed new algorithm for decision making in the face of the neurophysiological alarms during spinal deformity surgeries – oral presentation – symposium: new proposals for Tc-MEP interpretation in spinal deformities and intramedullary spinal cord tumor (MSCT) surgeries. In: 31st international congress of clinical neurophysiology. Washington, DC: IFCN; 2018. 21. Fu KM, Smith JS, Polly DW, Ames CP, Berven SH, Perra JH, Scoliosis Research Society Morbidity and Mortality Committee, et  al. Morbidity and mortality associated with spinal surgery in children: a review of the Scoliosis Research Society morbidity and mortality database. J Neurosurg Pediatr. 2011;7(1):37–41. PMID: 21194285. Available from: https://doi. org/10.3171/2010.10.PEDS10212. 22. Halsey MF, Myung KS, Ghag A, Vitale MG, Newton PO, Kleuver M.  Neurophysiological monitoring of spinal cord function during spinal deformity surgery: 2020 SRS neuromonitoring information statement. Spine Deform. 2020;8(4):591–6. PMID: 32451978. [cited 2020 May 25]. Available from: https://doi.org/10.1007/s43390-­020-­00140-­2. 23. Hamilton DK, Smith JS, Sansur CA, Glassman SD, Ames CP, Berven SH, Scoliosis Research Society Morbidity and Mortality Committee, et al. Rates of new neurological deficit associated with spine surgery based on 108,419 procedures: a report of the scoliosis research society morbidity and mortality committee. Spine. 2011;36(15):1218–28. PMID: 21217448. [cited 2011 Jul 1]. Available from: https://doi.org/10.1097/BRS.0b013e3181ec5fd9. 24. Hwang W, Lee J, Park J, Joo J. Dexmedetomidine versus remifentanil in postoperative pain control after spinal surgery: a randomized controlled study. BMC Anesthesiol. 2015;15:21. 25. Jarvis GJ, Strantzas S, Lipkus M, Holmes LM, Dear T, Magana S, et al. Responding to neuromonitoring changes in 3-column posterior spinal osteotomies for rigid pediatric spinal deformities. Spine. 2013;38(8):493–503. 26. Johnson T, Kale EB, Husain AM. Magnesium sulfate-induced motor evoked potential changes. Neurodiagn J. 2018;58(2):83–90. Available from: https://doi.org/10.1080/21646821.201 8.1469336. 27. Katharine Ker, Phil Edwards, Pablo Perel, Haleema Shakur, Ian Roberts; Effect of tranexamic acid on surgical bleeding: systematic review and cumulative meta-analysis. BMJ 2012;344:e3054. https://doi.org/10.1136/bmj.e3054. 28. Kothbauer KF, Vedran D, Epstein FJ. Motor-evoked potential monitoring for intramedullary spinal cord tumor surgery: correlation of clinical and neurophysiological data in a series of 100 consecutive procedures. Neurosurg Focus. 1998;4(5):3.

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29. Lall RR, Hauptman JS, Munoz C, Cybulski GR, Koski T, Ganju A, et al. Intraoperative neurophysiological monitoring in spine surgery: indications, efficacy, and role of the preoperative checklist. Neurosurg Focus. 2012;33(5):10. PMID: 23116090. Available from: https://doi. org/10.3171/2012.9.12235. 30. Langeloo DD, Journée HL, de Kleuver M, Grotenhuis JA. Criteria for transcranial electrical motor evoked potential monitoring during spinal deformity surgery A review and discussion of the literature. Neurophysiol Clin. 2007;37(6):431–9. PMID: 18083499. [cited 2007 Sep 5]. Available from: https://doi.org/10.1016/j.neucli.2007.07.007. 31. Laratta JL, Ha A, Shillingford JN, Makhni MC, Lombardi JM, Thuet E, et al. Neuromonitoring in spinal deformity surgery: a multimodality approach. Global Spine J. 2018;8(1):68–77. 32. Legatt AD, Emerson RG, Epstein CM, MacDonald DB, Deletis V, Bravo RJ, et  al. ACNS guideline: transcranial electrical stimulation motor evoked potential monitoring. J Clin Neurophysiol. 2016;33(1):42–50. PMID: 26756258. Available from: https://doi.org/10.1097/ WNP.0000000000000253. 33. Lieberman JA, Feiner J, Rollins M, Lyon R, Jasiukaitis P.  Changes in transcranial motor evoked potentials during hemorrhage are associated with increased serum propofol concentrations. J Clin Monit Comput. 2018;32(3):541–8. PMID: 28856576. [cited 2017 Aug 30]. Available from: https://doi.org/10.1007/s10877-­017-­0057-­4. 34. Lo YL, Dan YF, Tan YE, Nurjannah S, Tan SB, Tan CT, Raman S. Intraoperative motor-evoked potential monitoring in scoliosis surgery: comparison of desflurane/nitrous oxide with propofol total intravenous anesthetic regimens. J Neurosurg Anesthesiol. 2006;18(3):211–4. https:// doi.org/10.1097/01.ana.0000211007.94269.50. PMID: 16799350. 35. Loder RT, Thomson GJ, LaMont RL. Spinal cord monitoring in patients with nonidiopathic spinal deformities using somatosensory evoked potentials. Spine. 1991;16(12):1359–64. PMID: 1771465. Available from: https://doi.org/10.1097/00007632-­199112000-­00003. 36. Lyon R, Lieberman JA, Grabovac MT, Hu S. Strategies for managing decreased motor evoked potential signals while distracting the spine during correction of scoliosis. J Neurosurg Anesthesiol. 2004;16:67–170. 37. MacDonald DB.  Safety of intraoperative transcranial electrical stimulation motor evoked potential monitoring. J Clin Neurophysiol. 2002;19:416–29. 38. Macdonald DB, Skinner S, Shils J, Yingling C; American Society of Neurophysiological Monitoring. Intraoperative motor evoked potential monitoring - a position statement by the American Society of Neurophysiological Monitoring. Clin Neurophysiol. 2013;124(12):2291–316. https://doi.org/10.1016/j.clinph.2013.07.025. Epub 2013 Sep 18. PMID: 24055297. 39. Moura Filho JP, Bordalo-Rodrigues M, et al. What abdominal radiologists should know about extragenital endometriosis-associated neuropathy. Abdom Radiol. 2020;45(6):1818–28. 40. Nagarajan L, Ghosh S, Dilon D, Palumbo L, Woodland P, Thalayasingam P, et al. Interoperative neurophysiology monitoring in scoliosis surgery in children. Clin Neurophysiol Pract. 2019;25(4):11–7. 41. Nash CL, Lorig RA, Schatzinger LA, Brown RH.  Spinal cord monitoring during operative treatment of the spine. Clin Orthop Relat Res. 1977;156:100–5. 42. Nathan N, Tabaraud F, Lacroix F, Mouliès D, Viviand X, Lansade A, et  al. Influence of propofol concentrations on multipulse transcranial motor evoked potentials. Br J Anaesth. 2003;91:493–7. 43. Neira VM, Ghaffari K, Bulusu S, Moroz PJ, Jarvis JG, Barrowman N, et al. Diagnostic accuracy of neuromonitoring for identification of new neurologic deficits in pediatric spinal fusion surgery. Anesth Analg. 2016;123:1556–66. 44. Nuwer MR, Dawson EG, Carlson LG, Kanim LE, Sherman JE, et al. Somatosensory evoked potential spinal cord monitoring reduces neurologic deficits after scoliosis surgery: results of a large multicenter survey. Electroencephalogr Clin Neurophysiol. 1995;96(1):6–11. 45. Oro J, Haghighi SS. Effects of altering core body temperature on somatosensory and motor evoked potentials in rats. Spine. 1992;17:498–503.

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46. Owen JH. The application of intraoperative monitoring during surgery for spinal deformity. Spine. 1999;24(24):2649–62. 47. Padberg AM, Wilson-Holden TJ, Lenke LG, Bridwell KH.  Somatosensory  – and motor  – evoked potential monitoring without a wake-up test during idiopathic scoliosis surgery. An accepted standard of care. Spine. 1998;23(12):1392–400. PMID: 9654631. Available from: https://doi.org/10.1097/00007632-­199806150-­00018. 48. Pahys JM, Guille JT, Andrea LP, Samdani AF, Beck J, Betz RR.  Neurologic injury in the surgical treatment of idiopathic scoliosis: guidelines for assessment and management. J Am Acad Orthop Surg. 2009;17(7):426–34. PMID:19571298. Available from: https://doi. org/10.5435/00124635-­200907000-­00003. 49. Parikh P, Cheongsiatmoy J, Shilian P, Gonzalez AA.  Differences in the transcranial motor evoked potentials between proximal and distal lower extremity muscles. J Clin Neurophysiol. 2018;35(2):155–8. 50. Pastorelli F, Di Silvestre M, Plasmati R, Michelucci R, Greggi T, Morigi A, et al. The prevention of neural complications in the surgical treatment of scoliosis: the role of the neurophysiological intraoperative monitoring. Eur Spine J. 2011;20(1):105–14. 51. Pechstein U, Nadstawek J, et al. Isoflurane plus nitrous oxide versus propofol for recording of motor evoked potentials after high frequency repetitive electrical stimulation. Electroencephalogr. Clin. Neurophysiol., 1998;108(2):175–81. 52. Pelosi L, Lamb J, Grevitt M, Webb JK, Blumhardt LD, et al. Combined monitoring of motor and somatosensory evoked potentials in orthopaedic spinal surgery. Clin Neurophysiol. 2002;113(7):1082–91. 53. Polly DW Jr, Rice K, Tamkus A. What is the frequency of intraoperative alerts during pediatric spinal deformity surgery using current neuromonitoring methodology? A retrospective study of 218 surgical procedures. Neurodiagn J. 2016;56(1):17–31. PMID: 27180504. Available from: https://doi.org/10.1080/21646821.2015.1119022. 54. Quinones-Hinojosa A, Gulati M, Lyon R, et al. Spinal cord mapping as an adjunct for resection of intramedullary tumors: surgical technique with case illustrations. Neurosurgery. 2002;51:1199–206. discussion 1206–7. 55. Schwartz DM, Auerbach JD, Domans JP, Flynn J, Drummond DS, Bowe JA, et  al. Neurophysiological detection of impending spinal cord injury during scoliosis surgery. J Bone Joint Surg Am. 2007;89:2440–9. 56. Segura MJ, Talarico ME, Noel MA.  A multiparametric alarm criterion for motor evoked potential monitoring during spine deformity surgery. J Clin Neurophysiol. 2017;34(1):38–48. https://doi.org/10.1097/wnp.0000000000000323. PMID: 28045856. 57. Seki H, Ideno S, Ishihara T. et al. Postoperative pain management in patients undergoing posterior spinal fusion for adolescent idiopathic scoliosis: a narrative review. Scoliosis 13, 17 (2018). https://doi.org/10.1186/s13013-018-0165. 58. Sethi R, Bohl M, Vitale MG. State-of-the-art reviews: safety in complex spine surgery. Spine Deform. 2019;7:657–68. 59. Shao J, Lee BS, Pelle D, Lee MY, Savage J, Tanenbaum JE, et al. Intraoperative multimodal monitoring in pedicle subtraction osteotomies of the lumbar spine: a narrative literature review. Clin Spine Surg. 2019;32(4):137–42. 60. Skinner SA, Holdefer RN. Intraoperative neuromonitoring alerts that reverse with intervention: treatment paradox and what to do about it. J Clin Neurophysiol. 2014;31(2):118–26. PMID: 24691228. Available from: https://doi.org/10.1097/WNP.0000000000000030. 61. Spielholz NI, et al. Somatosensory evoked potentials during decompression and stabilization of the spine: methods and findings. Spine. 1979;4(6):500–5. 62. Takata Y, Sakai T, Higashino K, Matsuura T, Suzue N, Hamada D, et al. State of the art: intraoperative monitoring in spinal deformity surgery. J Med Investig. 2015;62(3–4):103–8. 63. Thirumala PD, Huang J, Thiagarajan K, Cheng H, Balzer J, Crammond DJ, et al. Diagnostic accuracy of combined multimodality somatosensory evoked potential and transcranial motor

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evoked potential intraoperative monitoring in patients with idiopathic scoliosis. Spine. 2016;41(19):1177–84. 64. Thuet ED, Winscher JC, Padberg AM, Bridwell KH, Lenke LG, Dobbs MB, et al. Validity and reliability of intraoperative monitoring in pediatric spinal deformity surgery: a 23-year experience of 3436 surgical cases. Spine. 2010;35(20):1880–6. 65. Tsikiros AI, Duckworth AD, Henderson LE, Michaelson C. Multimodal intraoperative spinal cord monitoring during spinal deformity surgery: efficacy, diagnostic characteristics, and algorithm development. Med Princ Pract. 2020;29:6–17. 66. Turner JD, Eastlack RK, Mirzadeh Z, Nguyen S, et al. Fluctuations in spinal cord perfusion during adult spinal deformity correction identify neurologic changes: proof of concept. World Neurosurg. 2016;85(365):6–80. 67. Uncini A, Santoro L. The electrophysiology of axonal neuropathies: more than just evidence of axonal loss. Clin Neurophysiol. 2020;131(10):2367–74. PMID: 32828039. [cited 2020 Aug 10]. Available from: https://doi.org/10.1016/j.clinph.2020.07.014. 68. Vauzelle C, Stagnara P, Jouvinroux P.  Functional monitoring of spinal cord activity during spinal surgery. Clin Orthop Relat Res. 1973;9:173–8. PMID: 4146655. Available from: https:// doi.org/10.1097/00003086-­197306000-­00017. 69. Villas C, Barrios RH. Congenital absence of the pedicles and the neural arch of L2. Eur Spine J. 1997;6(5):354–6. PMID: 9391810; PMCID: PMC3454610. Available from: https://doi. org/10.1007/BF01142686. 70. Vitale MG, Skaggs DL, Pace GI, Wright ML, Matsumoto H, Anderson RCE, et al. Best practices in intraoperative neuromonitoring in spine deformity surgery: development of an intraoperative checklist to optimize response. Spine Deform. 2014;2(5):333–9. PMID: 27927330. [cited 2014 Aug 27]. Available from: https://doi.org/10.1016/j.jspd.2014.05.003. 71. Walker CT, et al. Neuroanesthesia guidelines for optimizing transcranial motor evoked potential neuromonitoring during deformity and complex spinal surgery: a Delphi consensus study. Spine. 2020;45(13):911–20. 72. Wu Y, Cohen D, Tellez MJ, DiGiacinto GV, Barquero AV, Ulkatan S. Application of different thresholds for instrumentation device testing in minimally invasive lumbosacral spine fixation. J Clin Neurosci. 2020;72:224–8. PMID: 31866354. [cited 2019 Dec 19]. Available from: https://doi.org/10.1016/j.jocn.2019.11.036. 73. Xue L, Luo S, Ding H, Zhu Y, Liu Y, Huang W, et al. Risk of spinal cord ischemia after thoracic endovascular aortic repair. J Thorac Dis. 2018;10(11):6088–96. PMID: 30622780 [cited 2018 Nov]. Available from: https://doi.org/10.21037/jtd.2018.10.99. 74. Yang J, Skaggs DL, Chan P, Shah SA, Vitale MG, Neiss G, et al. Raising mean arterial pressure alone restores 20% of intraoperative neuromonitoring losses. Spine. 2018;43(13):890–4. PMID: 29049087. Available from: https://doi.org/10.1097/BRS.0000000000002461. 75. Ziewacz JE, Arriaga AF, Bader AM, Berry WR, Edmondson L, Wong JM, et al. Crisis checklists for the operating room: development and pilot testing. J Am Coll Surg. 2011;213(2):212–7. Erratum in: J Am Coll Surg. 2012;215(2):310. Dosage error in article text. PMID: 21658974. [cited 2011 Jun 11]. Available from: https://doi.org/10.1016/j.jamcollsurg.2011.04.031. 76. Ziewacz JE, Berven SH, Mummaneni VP, Tu TH, Akinbo OC, Lyon R, et  al. The design, development, and implementation of a checklist for intraoperative neuromonitoring changes. Neurosurg Focus. 2012;33(5):11. PMID: 23116091. Available from: https://doi.org/10.317 1/2012.9.FOCUS12263. 77. Zuckerman SL, Forbes JA, Mistry AM, Krishnamoorthi H, Weaver S, Mathews L, et  al. Electrophysiologic deterioration in surgery for thoracic disc herniation: impact of mean arterial pressures on surgical outcome. Eur Spine J. 2014;23:2279–90.

Chapter 23

Lumbar Interbody Fusion Surgeries: LIFS Ricardo José Rodriguez Ferreira, Marcus Vinícius Magno Gonçalves, Emília Caram Bordini, and Alexandre Fogaça Cristante

Abbreviations ALIF Anterior Interbody Fusion EMG Electromyography EMGfr Electromyography Free Running EMGst Electromyography Stimulated EMGtg Electromyography Triggered IONM Intraoperative Neurophysiological Monitoring IONMm Multimodal Intraoperative Neurophysiological Monitoring IONMu Unimodal Intraoperative Neurophysiological Monitoring LIF Lumbar Interbody Fusion

R. J. R. Ferreira (*) · E. C. Bordini AACD - Disabled Child Care Association, São Paulo, SP, Brazil Dr Ricardo Ferreira Clinic, São Paulo, SP, Brazil Spine Surgery Department at Orthopedics and Trauma Institute of Clinical Hospital of the University of São Paulo Medical School, São Paulo, SP, Brazil M. V. M. Gonçalves Neurologist and Neurophysiologist, Neurology at the University of the Region of Joinville (UNIVILLE), Joinville, Brazil A. F. Cristante Spine Surgery Department at Orthopedics and Trauma Institute of Clinical Hospital of the University of São Paulo Medical School, São Paulo, SP, Brazil © The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 S. M. Verst et al. (eds.), Intraoperative Monitoring, https://doi.org/10.1007/978-3-030-95730-8_23

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Lateral Interbody Fusion Oblique Lumbar Interbody Fusion Posterior Lumbar Interbody Fusion Somatosensory Evoked Potentials Transcranial Motor Evoked Potentials Transforaminal Lumbar Interbody Fusion

Surgeon’s Point of View Lumbar interbody fusion (isolated or associated with posterior arthrodesis) may be indicated for the treatment of various pathologies, including traumatic, neoplasic, and degenerative in origin. Several surgical access techniques have been developed over time to minimize complications and increase the fusion success rate, the main ones being: • • • • •

ALIF (former lumbar interbody fusion) OLIF (oblique lumbar interbody fusion) LLIF – XLIF (lateral lumbar interbody fusion/extreme lateral interbody fusion) TLIF (transforaminal lumbar interbody fusion) PLIF (posterior lumbar posterior lumbar interbody fusion)

The choice of technique to be used must take into account the surgeon’s experience, the underlying disease that leads to the treatment, as well as the lumbar level to be operated. The anatomical structures at risk vary considerably between each surgical access, and the main complications could be: • ALIF: vascular injury (mainly iliac vein) and superior hypogastric plexus injury (leading to premature ejaculation in men) • OLIF: excessive psoas muscle retraction (leading to thigh paresthesia and hip flexion weakness) • LLIF: lumbar plexus injury (usually temporary symptoms) through the psoas muscle • TLIF: damage to the dural sac and nerve roots (smaller compared to PLIF due to less distance) • PLIF: lesion of the dural sac and nerve roots (greater distance for disc space access) The use of IONM allows increasing the neurological safety of spinal column procedures. The evaluation during the passage of the pedicle screws gives the surgeon a functional parameter of good positioning, thus reducing the risk of neurological damage. Continuous assessment during the manipulation of neurological structures (dural sac and/or nerve root in the case of TLIF/PLIF, or lumbar plexus in the case of XLIF/LLIF) allows the surgeon to minimize actions that could result in further neurological damage.

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Effective communication between neurophysiologist and surgeon is very important for quick decision-making during surgery and can change the outcome of neurological status. Therefore, from the surgeon’s point of view, IONM is a great ally for the success of lumbar interbody fusion procedures and should, whenever possible, be used.

I ntraoperative Neurophysiological Monitoring to LLIF Techniques The surgical techniques known as LIF (lumbar interbody fusion), LLIF (lateral), ALIF (anterior), OLIF (Oblique), PLIF (posterior), and TLIF (transforaminal) (Figs.  23.1 and 23.2) consist of minimally invasive procedures. The LLIF techniques consist of surgical instrumentation through a direct lateral retroperitoneal approach, used as an alternative to traditional open surgeries. Numerous advantages are recognized for minimally invasive techniques, but neurological complications arising from this type of surgical procedure have been reported in several studies [1–7]. The neuroanatomical proximity of the lumbar plexus in relation to the iliopsoas muscle, used as one of the access pathways, increases the risk of secondary neurological complications when using this technique [1]. Le et al. [2] found the prevalence of 10.7–26.1% for immediate postoperative paresthesia and 54.9% for ipsilateral weakness of muscles innervated by the femoral nerve. One of the possible causes for the high frequency of neurological lesions is due to the variability of lumbar plexus topography [3], shown using the neurography (tractography) technique through a nuclear magnetic resonance of the lumbar plexus [4]. Fig. 23.1 Surgical approaches to the lumbar spine for interbody fusion techniques. The five approaches are shown schematically

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Fig. 23.2  Anterior, lateral, and oblique lumbar interbody fusion

Multimodal IONM (IONMm), by means of its two stages of mapping and monitoring, should yield precise information to the surgeon about the functioning of the peripheral and central nervous systems involved with this access pathway. The real-­ time feedback lets surgeons correlate their actions at a given surgical step to the IONM findings, allowing them to interrupt maneuvers, retreat, and, with this, prevent neurological lesions. This type of information is supplied to the surgical team throughout all stages of the procedure, including the positioning of both upper and lower limbs of the patient, opening of the transpsoas access, introduction of the first dilators, opening and maintenance of the tricuspid retractor, discectomies, and, lastly, placement of the proof and definitive cage. Moreover, the safety profile, the efficacy, and the cost-effectiveness of IONM must be taken into consideration [5]. The most used modalities in IONM during spinal surgery include somatosensory evoked potentials (SEP), transcranial motor evoked potentials (TcMEP), and electromyography (EMG), which can be free run (EMGfr) and stimulated (EMGst). However, the EMGst technique, which is claimed to be the most important neurophysiological test during the access pathway, only detects the approximation of the surgeon’s instruments to neural structures. Indeed, it determines, through the depolarization threshold found, the distance between them, which should be analyzed by the team if it is within a safety range. However, EMGst is not a monitoring technique, but rather only a mapping tool. This means that EMGst detects the proximity to neural structures but does not allow the monitoring of lesions occurrence. For this reason, its use is restricted to the first moment of surgery. An example is by the implantation of the first dilators followed by the tricuspid retractor, which is assessed by stimulating its three blades: cranial, caudal, and posterior (the latter of which is the most important). The advance through the psoas muscle poses a risk to the nearby femoral nerve (Fig. 23.3).

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Fig. 23.3  EMG-st: stimulation of the tricuspid retractor in LLIF surgeries

Given these facts, we highlight that unimodal IONM (IONMu) is incomplete to diagnose most lesions that could occur in this pathway. Thus, it is essential to additionally monitor using the evoked potentials above mentioned (IONMm). Riley et al. [6] published a non-randomized retrospective analysis of 479 procedures operated using the LLIF technique. The group that used TcMEP presented lower rates of immediate postoperative neurologic deficit (22.3%), including sensory and motor deficits, when compared to the group that used EMG alone, with 40.4% of complications. The prevalence of immediate motor deficit was 5.7% in the group that used TcMEP versus 17.1% in the group that used EMG alone, and the rate of irreversible motor deficit was significantly lower in the group that used TcMEP (6.9%) versus the group that used EMG alone (11.0%). The authors concluded that TcMEP seems to be the most effective monitoring modality to prevent permanent neurological lesions in the LLIF approach [6]. Sutter et al. [7] compared the different methods described previously in IONM regarding the detection of neurological complications during spinal surgery in 2728 patients that underwent LLIF.  The sensitivity and specificity of IONMm were 93.0% and 99.1%, respectively. For IONMu, sensitivity rates ranged between 13% and 81% to detect neurological complications. The authors concluded that IONMm was more effective and precise in the neurophysiological assessment during spinal surgery for reducing neurological complications, in comparison to the IONMu. We recommend that IONMm be conducted in all orthopedic surgeries, including those applying LLIF techniques. Thus, the TcMEP and SEP modalities should always be used, routinely, to reduce the risk of reversible and irreversible neurological damage. Hence, in face of this context, we suggest the adoption of seven fundamental steps for IONMm of surgeries using the LLIF technique: 1. The patient is correctly positioned with table folds aiming to vertebral level optimized access. Through radioscopy, the surgeon chooses the adequate location to transverse the psoas muscle. Initially, using a stimulator probe measuring 25 cm in length, the surgeon introduces the probe to map and locate nerves, especially

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those that are most exposed: genitofemoral and femoral nerves. Then, surgical reamers (usually three) are introduced and stimulated, applying pulses lasting 0.1 ms/100 us. We use EMGst to correlate the intensity of stimulation with the distance between the stimulator/reamers to neural structures. In our protocol, the decision-making is based on the following parameters (Fig. 23.4): • Green: ≥10 mA: Safe, not requiring repositioning. • Yellow: 5.0–10  mA: Caution, repositioning is decided by the surgeon in agreement with images and the concrete possibility of achieving a better position. • Red: ≤5.0 mA: Danger, we recommend reposition. It should be considered that polyneuropathies may have higher depolarization thresholds in EMGst. This can lead to false negatives, due to the difficulty in determining the exact distance between the instrument and the nerves and may result in lesions still during the first stage of surgery. Therefore, we suggest a change of paradigm that has not yet been proposed in the current literature, but that is necessary for a more adequate neurophysiological mapping study. The stimulator probe must be thin and with adequate length (25 cm) and should be the first instrument to be introduced in the psoas muscle. The probe will carry out the mapping through direct stimulation of the lumbar plexus nerves, reducing the occurrence of false results that can be generated through indirect stimulation from the dilators. Of note, the genitofemoral nerve is superficial to the psoas muscle. 2. TcMEP of the muscles innervated by the lumbar plexus nerves, namely, genitofemoral (cremaster muscle), obturator (adductor magnus muscle), and femoral (iliopsoas and quadriceps muscles) should be performed throughout the intraoperative period. It aims to diagnose neurological lesion due to rupture, ischemia, or traction. As previously mentioned, lesions cannot be identified by EMGst because it is solely a mapping/locator tool. Therefore, if a lesion is caused during the introduction of any instrument, EMGfr may show signs of mechanical depolarization; however, to diagnose the lesion, and to determine if it was partial or complete, MEPs are necessary. Of note, a muscle atlas is available in Chap. 3. 3. Add TcMEP of the muscles innervated by the external and internal branches of the sciatic nerve, bilaterally, since there is a great risk of lesion, due to the

Fig. 23.4 EMG-ST responses schematically grouped by color. Green: Safe, Yellow: Caution, Red: Danger

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p­ rolonged hold on lateral position. In this type of surgery, special attention on the consequences of the patient’s position is necessary because the lower limbs are routinely fixed with bandages to maintain perfect lateralization of the patient on the surgical table. Additionally, exaggerated traction can occur over the nerves if the table is folded incorrectly, meaning that the table fold should occur ideally at the level of the femoral trochanter. If there is an excessive slope in this fold, greater risk is posed on the lumbosacral plexus. With the experience acquired with IONMm during transpsoas lateral pathway access, we have frequently observed deterioration in TcMEP potentials not only in the territory of lumbar plexus nerves, but also in the territory of sacral plexus nerves (Fig. 23.5). In practice, we occasionally suggest to the surgeon a decrease in the angle of the table folding, especially in cases where this angle must be increased to move the iliac wing away from the surgical access. Indeed, in this situation, neurophysiological alterations may be seen in the external portion of the sciatic nerve. 4. TcMEP should be carried out every 5 min after the tricuspid retractor is opened. Closing the retractor is recommended if TcMEP presents a significant amplitude reduction greater than 50% in the muscles of the lumbar plexus territory. It is known that after 20–25  min of the opening of the tricuspid retractor, motor responses begin to decrease, regardless of the lack of activity in EMGfr. Thus, in our protocol 20–25 min should be the maximum time for the retractor to remain open. The surgeon may need more time, depending on his learning curve. Therefore, the greater the experience of the surgeon, the shorter the time in which the retractor remains open, with consequent reduction of the risks. This time is also correlated with the previous status of the peripheral nerves. In other words, similar to what was mentioned regarding the EMGst, patients with polyneuropathies require closer attention during this stage, since there may be a decrease in time length for MEP alterations to emerge. Thus, in this specific group of patients, it may eventually be necessary to close the tricuspid before reaching 20–25  min, as established for the general population (Figs.  23.6 and 23.7). 5. Routine SEP of the saphenous nerves bilaterally should be performed since it provides sensitive information on the femoral territory. Indeed, the most common sensitive lesion in the LLIF technique is the femoral nerve lesion [2]. 6. Carrying out TcMEP and SEP of bilateral ulnar nerve territory is imperative due to the risks posed by prolonged lateral patient’s decubitus. The compromise may occur at the elbow, brachial plexus, or cervical roots, due to the maintenance of the patient’s head position in lateral rotation. 7. We recommend femoral nerve H Reflex with stimulation in the inguinal region and recording in the rectus femoris muscle. The reason is that the sensory loop of the H reflex is shorter, and it does not need the averaging used in the SEPs (Fig. 23.8). Yet, it may be difficult to obtain the H reflex due to the amplitude of the response. To overcome this problem, we increase the distance of the recording electrodes [8].

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Fig. 23.5  Tc-MEP during LLIF surgery. (a) Red squares: amplitude drop of the Tc-MEP in the femoral territory; (b) green square: recovery of Tc-MEP responses in the femoral territory; (c) blue square: amplitude drop of the Tc-MEP in the lombossacral plexus territory

 he Increase of the Inter-electrode Distance in the Quadriceps T Femoris Technique [8] The TcMEP responses of the proximal muscles are reduced in amplitude when compared to the distal muscles [9–13]. This is due to three factors: (1) less representation in the cortex and corticospinal motor tract [9, 13, 14]; (2) greater inhibitory action on the motor neurons of the proximal muscles [14, 15], and (3) greater number of muscle fibers per motor unit in the proximal muscles [16, 17].

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Fig. 23.6  Saphenous nerve – SSEP. Transient amplitude drop during LLIF surgery

Fig. 23.7  Tc-MEP during LLIF surgeries. (a) Red square: transient drop of amplitude responses in the femoral nerve territory (muscles: iliopsoas, rectus femoris, adductor magnus); (b) blue square: gradual improvement of Tc-MEP responses of the femoral nerve after releasing the retractor

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Fig. 23.8  H reflex – femoral nerve. (a) Stimulus electrodes; (b) recording electrodes in the rectus femoris muscle; (c) H reflex of the femoral nerve, left and right. In the picture, it is possible to visualize the M and H responses

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Fig. 23.9  Increase of the inter-electrode distance in the quadriceps femoris technique. (a) Myotome recording montage, with 4 cm (REC 1) and 10 cm (REC 2) distance. (b) and (c) Tc-MEP responses, left and right lower limb, respectively. The responses are significantly greater in amplitude with 10 cm of inter-electrode distance

Parikh et al. [16] found similar results in the study of the TcMEPS and electrical stimulation of lower limbs [12]. Also, based on electroneuromyography studies of sensory and motor conduction, it is known that an increase in the distance between electrodes leads to an increase in the amplitude of the responses [17–20]. Recently, we addressed this issue regarding TcMEP of quadriceps [8], by analyzing 106 patients (212 limbs). The increase in the inter-electrode distance from 4 to 10 cm showed an increase in the Tc-MEP amplitude in all cases evaluated (Fig. 23.9). For this reason, we successfully applied this concept for the intraoperative femoral H reflex.

Prone Position for LLIF A new positioning technique for performing LLIF surgeries called “prone position” has recently been described. The benefits would be a better anatomical position of the psoas muscle and lumbar plexus, consequently with enhanced safety regarding neurological injuries related to LLIF instrumentation. Additionally, if a posterior approach is needed, the patient is already positioned [21].

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I ntraoperative Neurophysiological Monitoring to ALIF Techniques The anterior approach of the lumbar spine (ALIF) for decompression and implantation of lumbar prosthesis or cage is used for the treatment of the lumbosacral spine. Both implants aim to improve and maintain the intervertebral space. The prosthesis maintains mobility in the treated segment and the cage acts as an element for arthrodesis. The anterior approach is made through an abdominal incision, which can be median longitudinal or transverse suprapubic (Fig. 23.10). The main advantages of this approach are the greater spine exposure and direct access to the intervertebral disc, reduced muscle retraction, less blood loss, and reduced intraoperative time [22–25]. One of the major concerns regarding ALIF is the risk to the intraperitoneal and retroperitoneal vessels and to other structures (Fig. 23.11), which may need to be Fig. 23.10 Abdominal incisions in the anterior approach of the lumbar spine surgery. The types of incisions and the level of interest of the surgery are shown schematically. (Image: Courtesy of Aecio Rubens Dias Pereira Filho, MD [11])

lliac spine

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Fig. 23.11  Vessels and retroperitoneal structures. (Image: Courtesy of Aecio Rubens Dias Pereira Filho, MD [11])

Left ureter

Gonadal vessels

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repaired by a general, urological, or vascular surgeon on short notice [22]. Among the adverse events, there are neurological lesions, retrograde ejaculation, surgical site infection, ureter damage, and abdominal muscle injury [22–28]. For this reason, this technique has always brought some apprehension to the spine surgeons. Yet, ALIF has become increasingly popular due to the possibility of the aid of an “access surgeon,” ensuring greater safety to the surgery [23, 24]. Even so, there are still risks in this approach like vascular injury up to 18.1% [27]. Most frequently laceration affects the left common iliac vein during the vascular retraction step. Arterial injuries occur in 0.45% of the cases, far less frequently than venous injuries [28]. The abdominal arteries are more elastic and more easily movable than the veins; for this reason they are less likely to be injured by mobilization and retraction. The risk of damage to the left iliac vein is higher in surgeries performed in the lumbar levels above L5 [27, 28], when compared to surgeries performed at the lower lumbar levels. The reason is the anatomy of the iliac vein confluence, which usually occurs at the L5 vertebral body level, which makes the L5-S1 level safer [23, 29, 30] (Fig. 23.12). Yet, anatomical variations of the iliac arteries and veins, including different levels of the bifurcation of these vessels [23, 29], may lead to greater risks of vascular impairment, even in surgeries at the L5-S1 level. For this reason, sometimes it may be useful to perform a preoperative angiographic exam before the ALIF [30]. During the retraction of the iliac vessels, venous congestion may occur, resulting in an increased endoneural pressure [31]. Both arterial insufficiency and venous stasis can lead to ischemia of peripheral nerves and consequent neurophysiological

23  Lumbar Interbody Fusion Surgeries: LIFS Fig. 23.12  Anterior access of the lumbosacral spine and its correlation with the iliac vessels. In this schematic figure, the greatest technical difficulty can be seen, with the need for greater vessel retraction when approaching the superior levels of lumbassacral spine (L2/L3, L3/L4, and L4/L5). The L5/S1 level is most often located at the confluence of the veins/bifurcation of the iliac arteries; therefore, it needs little or no retraction. (Image: Courtesy of Aecio Rubens Dias Pereira Filho, MD [11])

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b alteration. The sensory axons are more susceptible to hemodynamic changes than the motor axons [32, 33]. Consequently, changes in SEP precede (Fig.  23.13) changes in the TcMEP responses (Fig. 23.14). Hence, IONMm should always be performed since it allows the early diagnosis of vascular impairment and may lead to vessel retraction removal. The return of responses to baseline levels (reversibility maneuver) proves that IONM changes are “true-positive” findings. It aims to prevent the development of more severe vascular impairment and neurological injuries. Accordingly, we suggest the adoption of fundamental steps for IONMm for surgeries using the ALIF technique: 1. Patient should be prepared while in dorsal decubitus, with the upper limbs crossed over the chest. The myotomes of choice will depend on the lumbar levels to be treated and the external anal sphincter monitoring is mandatory. 2. Record SEP and MEP baselines from the four limbs. 3. Next, the anesthetist may use neuromuscular blockers during the exposure of the abdominal field because of the difficulties in accessing the peritoneum in unrelaxed patients. It is suggested to control the neuromuscular blockage with the use of TOF (Train of Four), with a target of 50%.

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Fig. 23.13  SEP: transient amplitude drop of SEP cortical responses during the ALIF procedure. The amplitude drop is seen in both lower limbs, but is more pronounced in the left lower limb

Fig. 23.14  Tc-MEP: transient amplitude drop of Tc-MEP responses during the ALIF procedure. The amplitude drop is shown in the myotomes in the left sciatic nerve territory

4. During the vertebral approach, IONM should be continuously performed and EMGfr should be interspersed with SEP and Tc-MEP. 5. Tc-MEP and SEP should be recorded after implant (cage or disc prosthesis) placement. 6. Tc-MEP changes, with amplitude deterioration greater than 50%, if considered true positives, should be valued. If secondary to vascular etiology, they may be

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reversed by releasing the iliac vessel retractors. However, they may be due to direct neural tissue injury (during discectomy) or indirect injury (due to over distraction of the implant). Usually, concerning the L5-S1 level approach procedures, if at the end of the surgery the Tc-MEP changes remain, it may be secondary to check on the L5 root. The occurrence of posterior foraminal compression by the superior articular process of the inferior vertebra must be evaluated [34] (Fig. 23.15). In these situations, posterior decompression may be considered (Fig. 23.16).

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Fig. 23.15  Superior articular process of the inferior vertebra. (a) and (b) Radiological confirmation and (c) anatomical component, surgically resected

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Fig. 23.16  Tc-MEP response changes in the right L5 root (“MD3”) during lumbar surgery with the anterior and posterior approach. (a) Tc-MEP responses at the end of the anterior approach. (b) Significant amplitude deterioration in Tc-MEP responses, at the beginning of the posterior approach. (c) Improved Tc-MEP responses after posterior decompression

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Final Statements The use of multimodal IONM is the most adequate protocol to monitor neural integrity [6], but unfortunately, they are not widely used during surgeries applying the LLIF/ALIF techniques. We recommend the use of IONMm in all spinal surgeries. From a legal aspect in Brazil as in other countries, IONM must be conducted by a physician with adequate training to carry out the procedure. Indeed, in Brazil, non-compliance with this law incurs an illegal practice of medicine, which can lead to legal issues to the surgical team and hospital managers [35]. Remote monitoring, as practiced in several countries, is not permitted according to Brazilian laws. Therefore, it is mandatory that an in-site trained physician perform the IONM. The surgeon, his assistants, and the anesthesiologist are not allowed to perform concomitant neurophysiology monitoring. More details in this subject were detailed in Chap. 2.

Conclusion Despite the many advantages of minimally invasive surgery, many studies report neurological complications in this type of procedure. For this reason, the use of multimodal IONM is recommended in all LIF surgeries. The objective of multimodal IONM is to guarantee and assure to the surgical team a reduced rate of partial or permanent neurological complications [36].

References 1. Kepler CK, Bogner EA, Herzog RJ, et al. Anatomy of the psoas muscle and lumbar plexus with respect to the surgical approach for lateral transpsoas interbody fusion. Eur Spine J. 2011;20(4):550–6. 2. Le TV, Burkett CJ, Deukmedjian AR, et al. Postoperative lumbar plexus injury after lumbar retroperitoneal transpsoas minimally invasive lateral interbody fusion. Spine (Phila Pa 1976). 2013;38(1):E13–20. 3. He L, Dong J, Liu B, et al. A MRI study of lumbar plexus in patients with degenerative lumbar scoliosis after extreme lateral interbody fusion. Zhonghua Yi Xue Za Zhi. 2014;94(3):178–81. Published Online First: 2014/04/16. 4. Quinn JC, Fruauff K, Lebl DR, et al. Magnetic resonance neurography of the lumbar plexus at the L4-L5 disc: development of a preoperative surgical planning tool for lateral lumbar transpsoas interbody fusion (LLIF). Spine (Phila Pa 1976). 2015;40(12):942–7. 5. Laratta JL, Shillingford JN, Ha A, et al. Utilization of intraoperative neuromonitoring throughout the United States over a recent decade: an analysis of the nationwide inpatient sample. J Spine Surg. 2018;4(2):211–9. 6. Riley MR, Doan AT, Vogel RW, et al. Use of motor evoked potentials during lateral lumbar interbody fusion reduces postoperative deficits. Spine J. 2018;18(10):1763–78.

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7. Sutter M, Eggspuehler A, Jeszenszky D, et al. The impact and value of uni- and multimodal intraoperative neurophysiological monitoring (IONM) on neurological complications during spine surgery: a prospective study of 2728 patients. Eur Spine J. 2019;28(3):599–610. 8. Bordini EC, Ferreira RJR, Germano CSB, Barretto LS, et  al. Significant improvement in Tc-MEP responses in quadriceps femoris muscles by the simple increase of the inter-­ electrode distance: solving a long time problem. Poster session. 2020 American Clinical Neurophysiology Society (ACNS) Annual Meeting. J Clin Neurophysiol. 2020;37(4):310–72. https://doi.org/10.1097/WNP.0000000000000698. 9. Palmer E, Ashby P.  Corticospinal projections to upper limb motoneurones in humans. J Physiol. 1992;448:397–412. 10. Lemon RN, Mantel GW, Muir RB. Corticospinal facilitation of hand muscles during voluntary movement in the conscious monkey. J Physiol. 1986;381:497–527. 11. Phillips CG, Porter R. The pyramidal projection to motoneurones of some muscle groups of the baboon’s forelimb. Prog Brain Res. 1964;12:222–45. 12. Bernhard CG, Bohm E. Cortical representation and functional significance of the corticomotoneuronal system. AMA Arch Neurol Psychiatry. 1954;72(4):473–502. 13. Buchthal F, Schmalbruch H. Motor unit of mammalian muscle. Physiol Rev. 1980;60(1):90–142. 14. Rothwell JC, Thompson PD, Day BL, et al. Motor cortex stimulation in intact man. General characteristics of EMG responses in different muscles. Brain. 1987;110(Pt 5):1173–90. 15. Wassermann EM, McShane LM, Hallett M, Cohen LG. Noninvasive mapping of muscle representations in human motor cortex. Electroencephalogr Clin Neurophysiol. 1992;85(1):1–8. 16. Parikh P, Cheongsiatmoy J, Shilian P, Gonzalez AA.  Differences in the transcranial motor evoked potentials between proximal and distal lower extremity muscles. J Clin Neurophysiol. 2018;35(2):155–8. 17. Zipp P. Effect of electrode geometry on the selectivity of myoelectric recordings with surface electrodes. Eur J Appl Physiol. 1982;50:35–40. 18. Eduardo E, Burke D.  The optimal recording electrode configuration for compound sensory action potentials. J Neurol Neurosurg Psychiatry. 1988;51(5):684–7. 19. Evanoff Jr V, Buschbacher RM. Optimal interelectrode distance in sensory and mixed compound nerve action potentials: 3- versus 4-centimeter bar electrodes. Arch Phys Med Rehabil. 2004;85(3):405–8. 20. Jonas D, Bischoff C, Conrad B. Influence of different types of surface electrodes on amplitude, area and duration of the compound muscle action potential. Clin Neurophysiol. 1999;110(12):2171–5. 21. Pimenta L, Amaral R, Taylor W, Tohmeh A, Pokorny G, Rodrigues R, Arnoni D, Guirelli T, Batista M. The prone transpsoas technique: preliminary radiographic results of a multicenter experience. Eur Spine J. 2021;30(1):108–13. https://doi.org/10.1007/s00586-­020-­06471-­y. Epub 2020 May 29. Erratum in: Eur Spine J. 2020. 22. Than KD, et al. Complication avoidance and management in anterior lumbarinterbody fusion. Neurosurg Focus. 2011;31(4):E6. 23. Pereira Filho ARD. Technique for exposing lumbar discs in anterior approach using Steinmann wires: arthroplasties or arthrodesis. World Neurosurg. 2021;148:189–95. 24. Jarrett CD, et al. Anterior exposure of the lumbar spine with and without an “access surgeon”: morbidity analysis of 265 consecutive cases. J Spinal Disord Tech. 2009;22(8):559–64. 25. Tropiano P, et al. Surgical techniques for lumbo-sacral fusion. Orthop Traumatol Surg Res. 2017;103:S151–9. 26. Reddy D, et al. Extensive deep venous thrombosis resulting from anterior lumbar spine surgery in a patient with iliac vein compression syndrome: a case report and literature review. Global Spine J. 2015;5:e22–7. 27. Inamasu J, et al. Review article. Vascular injury and complication in neurosurgical spine surgery. Acta Neurochir. 2006;48:375–87. 28. Brau SA, et al. Vascular injury during anterior lumbar surgery. Spine J. 2004;4(4):409–12.

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29. Jasani V, et al. The anatomy of the iliolumbar vein. A cadaver study. J Bone Joint Surg Br. 2002;84:1046–9. 30. Inamasu J, et al. Three-dimensional computed tomographic anatomy of the abdominal great vessels pertinente to L4-L5 anterior lumbar interbody fusion. Minim Invasive Neurosurg. 2005;48:127–31. 31. Rydevik BL, et al. The effects of compression on the physiology nerve roots. J Manip Physiol Ther. 1992;15(1):62–6. 32. Bostcock H. Differences in behaviour of sensory and motor axons following release of ischaemia. Brain. 1994;117(Pt 2):225–34. 33. Brau SA, et al. Nerve monitoring changes related to iliac artery compression during anterior lumbar spine surgery. Spine J. 2003;3(5):351–5. 34. Neal MT, Kalani MA, Lyons MK. A technical nuance to avoid lumbar five radiculopathy with anterior lumbar fusion and posterior instrumentation. Case Rep Orthop. 2021;2021:5514720. https://doi.org/10.1155/2021/5514720. 35. Brazilian Federal Council of Medicine. Resoluction number 2.136/2015. Official Diary of the Union; 2016. Section 1, p. 71. 36. Shilian P, et al. Overview of intraoperative neurophysiological monitoring during spine surgery. J Clin Neurophysiol. 2016;33(4):333–9.

Chapter 24

Cervical Spinal Surgery Ricardo José Rodriguez Ferreira, Patrícia Toscano, Emília Caram Bordini, and Arthur Werner Poetscher

Abbreviations BIS Bispectral Indicis DWILT D-Wave Interspinous Ligament Technique EMG Electromyography EMG-fr Electromyography Free Run EMG-st Electromyography Triggered IONM Intraoperative Neurophysiological Monitoring

R. J. R. Ferreira (*) · E. C. Bordini AACD - Disabled Child Care Association, São Paulo, SP, Brazil Dr Ricardo Ferreira Clinic, São Paulo, SP, Brazil Spine Surgery Department at Orthopedics and Trauma Institute of Clinical Hospital of the University of São Paulo Medical School, São Paulo, SP, Brazil P. Toscano Neurology Department, Ribeirão Preto Medical School of the University of São Paulo, Ribeirão Preto, SP, Brazil A. W. Poetscher Neurosurgery Department at Hospital Israelita Albert Einstein, São Paulo, SP, Brazil © The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 S. M. Verst et al. (eds.), Intraoperative Monitoring, https://doi.org/10.1007/978-3-030-95730-8_24

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Mean Arterial Pressure Motor Evoked Potential Muscle Motor Evoked potential Motor Unit Action Potential Somatosensory Evoked Potential Transcranial Motor Evoked Potential Train of Four

Surgeon’s Point of View IONM has become an essential tool in cervical spine decompression surgery. Although some controversy regarding the use of IOM for specific procedures may persist, tools that improve patient safety should not be dismissed. The spinal cord and cervical spine nerve roots are always at risk during cervical spine surgery. Damage to spinal nerve roots can lead to weakness of specific muscles in arms and hands, as well as hypoesthesia and neuropathic pain in correspondent dermatomes. Cervical spinal cord injury may cause a variety of syndromes, including tetraplegia and loss of sphincter control. Cervical spine approaches can be classified into anterior and posterior. When compression originates from anterior elements, such as intervertebral disc, osteophytes, posterior longitudinal ligament, and normal cervical lordosis is compromised, surgery is usually performed using an anterior approach. Posterior compression caused by ligamentum flavum hypertrophy or multilevel canal stenosis is commonly treated with posterior approaches. Spinal nerve impingements are often treated by anterior approaches, although for specific compressions a posterior foraminotomy may be the best option. Intraoperative monitoring should begin before the patient is positioned. Flexion or extension of the neck when positioning can worsen the compression on the spinal cord and cause catastrophic damage. During an anterior approach, the recurrent laryngeal nerve can also be monitored with an electrode at the endotracheal tube, reducing the risk of injury and hoarseness after surgery. During decompression, when removing the disc or perforating the bone near the dura, injury to the spinal cord or spinal nerve roots can occur. The next step, placing the cage or graft, can also be critical, as improper positioning can cause compression. The critical times for later approaches are decompression and screw placement. Decompression can be performed by removing small amounts of bone each time with the use of rongeurs or a drill. Some surgeons prefer to perform a laminotomy by cutting the laminae with a drill and removing the posterior elements en bloc. When a posterior decompression is associated with a posterior arthrodesis, each screw placement must be carefully monitored to avoid spinal nerve injury. Some patients may wake up with deltoid weakness, the so-called C5 syndrome. This is probably caused by stretching of the nerve root that can occur after decompression. Therefore, C5 should always be monitored.

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Cervical compressive myelopathy is a very fragile condition. Minor surgical trauma can lead to dramatic neurological worsening. The IONM team’s warnings should always be heeded. Surgery should be paused, the operative field reviewed, and anesthetic parameters checked.

Introduction One of the main applications of multimodal intraoperative neurophysiological monitoring (IONM) in spine surgery is cervical spine surgery. Its importance begins in the preoperative period, with the evaluation of the correct positioning of the patient, both in anterior and posterior approaches. Motor deficits may arise from positioning in a patient with vertebral canal stenosis associated or not with cervical myelopathy. In addition, IONM can detect pre-existing neurological deficits, prevent central and peripheral nervous system injuries, and prove successful decompression maneuvers. Specifically in the anterior approach of cervical spine surgeries, there is a need for additional evaluation of the recurrent laryngeal nerve and/or superior laryngeal nerve structures that may be at risk of injury in the exposure phase [1]. The effectiveness of somatosensory evoked potential (SSEP) and motor evoked potential (MEP) techniques and electromyography (EMG), individually and in combination, provide greater sensitivity for early detection of clinically significant neurological impairment [2, 4, 5]. The incidence of neurological deficits in cervical spine surgery has been relatively low, ranging from 0.2% to 3.2% [6]. Several groups have set out to study the events that determine truly positive neurological outcomes [7, 8].

Main Pathologies of the Cervical Spine Cervical spine can be approached by both anterior and posterior approaches, and the indications are numerous: 1. Degenerative diseases: herniated discs, arthrosis (osteophytosis), listhesis, vertebral canal stenosis, rheumatologic diseases (ankylosing spondylitis), myelopathy, radiculopathy 2. Trauma: fracture, dislocation, traumatic listhesis, whiplash injury with posterior ligament rupture 3. Vertebral and neuraxial tumors 4. Deformity: cervical kyphosis 5. Congenital: Arnold-Chiari 6. Chronic pain

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Approaches Cervical spine can be approached by an anterior approach, a posterior approach, or both at the same surgical time. Posterior approaches can be performed in open surgeries or minimally invasive (endoscopic) surgeries. The anterior approach, transoral or latero-anterior cervical, is indicated for: 1. Decompression – discectomy, osteophytes and intracanal fragments resection, corpectomy 2. Arthrodesis – graft, disc cage, body cage 3. Arthroplasty – disk prosthesis In the posterior approach, the main indications are: 1. Decompression – single or multiple laminotomy or laminectomy 2. Arthrodesis  – in situ, lateral mass screw, pedicle screws, sublaminar bands or wires 3. Endoscopic

Anterior Approach Advantage  The main advantage of the anterior approach versus the posterior approach is the possibility of better exposure of the vertebral body, disc space, posterior ligament, and access to the anterior portion of the spinal cord, allowing decompression and arthrodesis with minimal manipulation of the neurological structures. Disadvantage  Possible injuries by withdrawal and even direct trauma to vascular, neural, tracheal, and esophageal structures due to the approach route. These sentinel events are potentially catastrophic [9]. Preoperative Preparation  The patient is transferred from the transport stretcher to the operating table where he will be prepared by the anesthesiologist, neurophysiologist, and nurse. Anesthesia Orotracheal tube: Set the gauge to be used so that the neurophysiologist applies the adhesive electrode on the tube. Tube adhesive electrode: Adhesive electrodes should have two channels and the appropriate width for the chosen tube. If there is excess adhesive that could cover the electrode contacts, this excess part must be cut off (Fig. 24.1).

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Anesthetic protocol: Totally intravenous anesthesia is recommended, considering the preoperative neurophysiological tests with the patient at rest. Only after these tests and depending on the responses found is the patient’s definitive positioning performed. For more details on general anesthesia, refer to Chap. 5. Curarization: If necessary, the neuromuscular blockade should be done with succinylcholine, due to the rapidity of its elimination, or even rocuronium, which is rapidly reversed by Sugammadex®, in a few minutes. Bite protection: After intubation, the neurophysiologist does the bite protection with a specific bite-block device, like Tongard® – Healthnology [10] – Fig. 24.2 – or with gauze cushions, placed bilaterally between the molars, thus avoiding lesions to the tongue, cheek, lips, teeth, and the bite of the orotracheal tube itself.

Fig. 24.1  Demonstration of the application of adhesive laryngeal electrode to the orotracheal tube. Eventually, it is necessary to cut an excess adhesive of the electrode

Fig. 24.2 TongardR Healthnology – bite-block device

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Neurophysiology Tests • SSEP: Ulnar and median nerves MMSS; tibial nerve MMII at ankle level. • MEP/EMG: Myotomes of interest according to the level or levels to be addressed. Usually, the upper trapezius (C3/4), deltoid (C5), biceps (C6), triceps (C7) and fifth finger abductor (C8/T1), tibialis anterior (L4), and abductor hallucis (S2) muscles are used. It is also possible to evaluate the recurrent laryngeal nerve (vocal cords), especially when approaching lower levels  – C5/C6/C7, or the superior laryngeal nerve (cricothyroid m. – Fig. 24.3), important in surgery of higher levels  – C3/C4/C5. In specific cases, external anal sphincter recording (S2-S4) may be considered. • MEP – D-wave (in cases of the transoral route). (Note of the editors: exclusively authors’ experience). Preparation With the patient already anesthetized, proceed to apply the needle and surface electrodes on the patient. Corkscrew needle electrodes adapted to the scalp for both SSEP recordings and MEP stimulation by the 10/20 or 10/10 EEG system. Orotracheal tube already with electrode adapted as mentioned above. Positioning Upper limbs positioning: Position the patient with arms along the body, making sure the thumbs are facing up. This confers the anatomical resting position of the shoulders and prevents postoperative pain related to prolonged inadequate positioning (in internal or external rotation). Also, check on arms position to avoid ulnar or radial nerves compression. Definitive positioning: After performing the neurophysiological tests at rest and analyzing the responses, agree with the surgical team to place the cushion under the

Fig. 24.3  Technique for capturing the cricothyroid muscle with needle electrodes. The neurophysiologist inserts the electrodes, after proper degermation and skin preparation by the surgeon

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scapular waist and to perform shoulder traction with adhesive tape. It is important to note that excessive traction on the shoulders can cause brachial plexus injury [11]. Check on fibular nerve at the fibular head. This positioning allows, preoperatively, the radioscopic evaluation and localization of the correct level to be treated; intraoperatively, a surgical field that is more favorable for direct macro- or microscopic visualization and better evaluation of the vertebral levels on radioscopy, especially the more caudal ones such as C6/C7. Post-positioning Repeat the neurophysiological tests and compare with the results obtained at rest. Tests without deficit change: Authorizing the beginning of surgery. Tests with some deficient alteration: Neurophysiological and anesthetic checklist: In neurophysiological tests, check electrode connections and if stimulation parameters are correct. In the anesthetic tests, check mainly if decurarization is complete by train of four – TOF and if mean arterial pressure – MAP and hypnosis are at adequate levels, the latter with a bispectral indicis – BIS measurement greater than 45%. If any of these parameters is inadequate, correct and repeat the tests. If the neurophysiological and anesthetic checklist is adequate, it is a true positive, the surgical team must be informed, and the patient repositioned. Tests now without deficit change or 50%: It is our protocol to consider >50% the major criterion of warning, although others would consider deterioration >80% or loss of MEP [11]. In our institution, the start of surgery should be suspended until the tests return to baseline. If no return of responses to baseline or acceptable levels is observed (a drop of less than 50%), the procedure should be suspended. In severe cervical myelopathies, in walking patients, simple positioning in cervical extension may lead to loss of caudal responses at the level of compression or myelomalacia. In some cases, deterioration or loss of responses are observed exclusively for the lower limbs. Even reducing the extension caused by positioning, it is possible that the responses do not return to baseline. In these cases, the most prudent decision is to suspend the procedure. It is worth noting that in some cases, especially in myelopathies, positioning may exert deleterious effects on motor and/or sensory pathways insidiously. Thus, there may be a delayed decline in IONM responses [12]. In these situations, positioning should be reevaluated, possibly with the need to reduce cervical extension. Thus, given this context, we suggest the adoption of nine key steps for neurophysiological monitoring of anterior approach cervical spine surgeries. Intraoperative: Step by Step • Step 1: Exposure by anatomical planes – free run electromyography (EMG-fr) • Step 2: Pre-positioning of the caspar retractor – muscle MEP (mMEP) • Step 3: Post-placing and opening caspar – mMEP

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Step 4: Discectomy and decompression – EMG-fr Step 5: Cage tester placement – mMEP Step 6: Cage placement – mMEP and SSEP Step 7: Caspar removal – mMEP and SSEP Step 8: Plate placement (if cage is not “stand alone” type) – mMEP and SSEP Step 9: Closure by planes – mMEP and SSEP

Considerations • Step 1: Watch out for the occurrence of neurotonic discharges in the EMG-fr in the territory of the recurrent laryngeal/superior laryngeal nerves. If such discharges are observed, control mMEP of the laryngeal nerve should be performed (Fig. 24.4). If the mMEP responses are maintained, such discharges only mean nerve manipulation, and it is suggested to reduce the traction used in the soft tissue retractors. • Step 2: Perform an update of the baseline, prior to the opening of the caspar distractor. This confirms that the positioning (cervical extension) remains adequate, as well as the anesthetic protocol. • Step 3: This is the first maneuver of higher risk for spinal cord involvement, by indirect mechanism (distraction). In most cases, after the distraction, transient drops in mMEP/SSEP responses may be seen. If these changes remain or show drops >50%, it should be suggested that the distraction be reduced or the caspar retractor temporarily removed. • Step 4: This is the first step that can generate direct spinal cord or radicular trauma. If neurotonic discharges occur in the EMG-fr, they should be reported and, depending on their intensity, control with MEP should be performed. • Steps 5 and 6: These steps can generate direct and indirect trauma to the spinal cord. In this phase, the same phenomenon occurs as reported in step 3 (opening of the caspar and distraction); that is, a transient drop in responses is expected, and if it is not intense or permanent, there is no need for alarm. However, if there is a marked reduction in responses, the surgical team should be notified, and

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Fig. 24.4  Tc-MEP of the recurrent laryngeal nerve. (a) and (b) left and right sides, respectively

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removal of the disc cage/prosthesis is suggested. Reducing the height of the disc cage/prosthesis may be considered if these changes persist. It is worth noting that the transient changes reported in steps 3, 5, and 6 occur frequently, and not knowing about them can generate false alarms, causing stress on the surgical team and impacting the neurophysiologist’s credibility. • Steps 7, 8, and 9: Observe the responses obtained in the continuous IONM. If a reduction in responses is visualized, inform the surgical team, and suggest a review of the last maneuvers performed.

Posterior Approach Advantage  Posterior approach allows a wide view to spinal cord decompression in severe multi-segmental stenosis. It is also the option of choice when the anterior approach presents significant neurological risks. Disadvantages  It does not address pathologies involving the anterior compartment of the cervical spine; the dreaded C5 palsy occurs more commonly with posterior approach decompressions [13]. Preoperative Preparation  The patient is prepared on the transport stretcher, in dorsal decubitus, by the anesthesiologist, neurophysiologist, and nurse. Anesthesia  The same protocol is recommended as for the anterior approach, except for the monitoring of the recurrent/superior laryngeal nerve (not necessary in this approach). Neurophysiology Tests • SEP, mMEP, and EMG: Follow the same protocol cited for the anterior approach; in this case, the preoperative tests at rest will be on the transport stretcher in dorsal decubitus, and the post-positioning will be in ventral decubitus on the operating table. • MEP: It is our opinion that in cases of severe vertebral canal compromise, such as stenosis, myelopathies, and fractures, the use of the D-wave along with mMEP may be of great use in posterior approach cervical surgeries since there may be a reduction or absence of mMEP responses. The presence of a stable D-wave may allow the continuity of the surgical procedure. D-wave recording needs to be validated by other groups though.

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Positioning Definitive positioning: After performing the neurophysiological tests at rest in dorsal decubitus and analyzing the responses, agree with the surgical team to change the decubitus from dorsal to ventral. The positioning is done with the patient supporting the head on a cushion or coupled to a standard cranial stabilization system (Mayfield). Upper limbs positioning: The upper limbs will be along the body, observing that the thumbs are turned downwards. As mentioned in the anterior approach, but in opposite way, this gives the anatomical resting position of the shoulders and avoids postoperative pain related to prolonged, inadequate positioning. In some cases, the shoulders can be pulled with adhesive tape by the surgical team. This positioning allows, preoperatively, the radioscopic evaluation and localization of the correct level to be treated; intraoperatively, it maintains a surgical field more proper to direct visualization (macro or microscopic) and better evaluation of the vertebral levels in the radioscopy, especially those more caudal such as C6/7. Post final positioning Repeat the neurophysiological tests and then compare with the results obtained when resting in the dorsal decubitus position. Tests without deficient alteration: Authorizing the beginning of surgery. Tests with some deficient alteration: Neurophysiological and anesthetic checklist, as cited above. If the neurophysiological and anesthetic checklist is adequate, it is a true positive, the surgical team must be informed, and the patient repositioned. Tests now without deficit change or 50%: It attests that the repositioning did not have the expected effect. In this situation, the start of surgery should be suspended until the tests return to baseline. If no return of responses to baseline or acceptable levels are observed (a drop of less than 50%), the procedure must be stopped, the patient returned to supine position on the transport stretcher, and the tests repeated. As mentioned above, this protocol is performed in our institution (see section “Anterior Approach”). As a protocol, we suggest the recording with the same myotomes recommended for the anterior approach. In addition, because the surgery is performed in ventral decubitus, it is mandatory to include the quadriceps femoris due to the use of cushion in the anterosuperior iliac spines, preventing positioning injuries. Thus, we suggest the following fundamental steps for neurophysiological monitoring of posterior approach cervical spine surgeries. Intraoperative: Step by Step • • • • •

Step 1: Exposure by anatomical planes – EMG-fr, mMEP, and SSEP Step 2: Lateral mass screws and/or pedicle screws – mMEP and SSEP Step 3: Laminectomy/decompression – EMG-fr, mMEP, and SSEP Step 4: Rods placement – mMEP and SSEP Step 5: Closure by planes – mMEP and SSEP

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Considerations • Step 1: At this stage, pay attention to any changes in basal tests, as they may be secondary to positioning. • Step 2: The lateral mass screws do not need stimulation (EMGst), because their risk is exclusively vascular (vertebral artery). The pedicle screws, when present (usually C2 and C7), could be stimulated with the same technique as the thoracic screws (EMGst: train of 4 pulses, ISI 2 ms, duration 0.2 ms or 200 μs and intensity 7  mA or determined by the threshold of the instrumented pedicle). Both cases should be monitored with mMEP and SEP. • Step 3: At this stage it is critical to evaluate the dorsal column, with SSEP, as this is the main structure at risk. In our institution, if D-wave is indicated, the epidural catheter should be inserted after laminectomy. Specific authors’ experience. A careful evaluation of the mMEP is also important. In cases of multi-­ laminectomies or multi-laminotomies, a greater possibility of C5 palsy is described [13, 14]. If C5 palsy occurs, it can be diagnosed by abruptly falling mMEP responses in this territory, immediately after laminectomy or a few minutes after decompression. • Steps 4 and 5: Maintaining continuous monitoring with mMEP and SSEP.  If changes are observed, the last surgical step performed should always be reviewed.

Endoscopic Approach There is popularization and increasing expansion of endoscopic and minimally invasive surgeries for the treatment of cervical disc herniations and stenosis, with the advantages of minimal tissue damage, less blood loss, rapid recovery, and early hospital discharge. IONM plays an important role in preventing nerve injury. Endoscopic cervical surgery can present some technical difficulties, such as the restriction of visualization of the operative field with the inherent risks to neural tissue, and it requires a learning curve for the use of the endoscope. Some surgeons recommend using local anesthetics or regional anesthesia, keeping the patient awake. This option is more attractive to patients, who are discharged earlier from the hospital. However, this practice is controversial. The development of safer, modern general anesthesia techniques proves that the method is superior or similar to local anesthesia and that surgeons feel more comfortable operating on a sleeping patient [15]. In 2016, Ruetten corroborated these aspects by pointing out that general anesthesia allows for better positioning and clinical stability during the procedure, facilitating more complex maneuvers in the spinal canal [16]. Furthermore, local anesthesia is more frequently associated to respiratory depression, with the need for changing from prone to supine position and from local to general anesthetic regimen – with a consequent need of intubation [17]. The access approaches in endoscopic surgery are: transforaminal and interlaminar [18]. In interlaminar surgeries, IONM is already considered paramount, since, mandatorily, the patient will be under general anesthesia.

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IONM in endoscopic surgeries follows the same multimodal protocol, with EMG-fr and EMG-st, monitoring with SSEP and mMEP, and EEG to follow the level of hypnosis. Preoperatively, IONM can detect prior neurological impairment, providing an accurate diagnosis, as mentioned in the other avenues of approach. EMG-fr allows triggering of minimal instrument contact alerts with neural structures and mMEP demonstrates the effectiveness of decompression as well as the occurrence of neural damage. Thus, the general anesthesia protocol coupled with IONM offers a faster and safer procedure. The awake patient may present more discomfort and problems with positioning, leading to legal issues [19]. In the endoscopic approach, the preoperative care, positioning, and post-­ positioning follow the same parameters cited for the posterior approach, since the patient is positioned in ventral decubitus. Thus, the main intraoperative steps in endoscopic surgeries (transforaminal or interlaminar route) are suggested: Intraoperative: step by step • Step 1: Introduction of the endoscopic cannula – EMG-fr • Step 2: Drilling of the foramen and/or lamina – EMG-fr, EMG-st, mMEP, SSEP • Step 3: Discectomy/decompression – EMG-fr, EMG-st, mMEP, SSEP • Step 4: End of decompression and removal of instruments – EMG-fr, EMG-st, mMEP, SSEP Considerations • Step 1: Assess the occurrence of neurotonic discharges by the proximity of neural tissue. • Step 2 and 3: In addition to evaluating the EMG-fr, similarly, to step 1, mapping of neural structures can be done with EMG-st. For this, the surgeon should be offered a long stimulating probe, with a length above 40  cm (average size of endoscopic cannulas). SSEP and mMEP should also be performed intermittently, to diagnose potential neural lesions early. • Stage 4: At this stage, it is particularly important to perform mMEP for final recordings.

IONM Tests Applied to Cervical Spine Surgeries Motor Evoked Potential mMEP mMEP is obtained by transcranial electrical stimulation through corkscrew-type electrodes inserted in the scalp at C3/C4, C3/Cz, C4/Cz, and the combination of other positions in the quadripolar technique (international system 10–20), with slight anteriorization from 2 to 4 cm. Recording is done in the myotomes pertinent to each case, as mentioned in topic 1. In mMEP, the technique used is a train of 5–9

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pulses, with a pulse duration ranging from 50 us/0.05 ms to 500 us/0.5 ms (depending on the equipment); the intensity is varied and generally high, from 200 to 1000  V.  We recommend the use of supra-maximal intensity because it makes it easier to observe changes in the amplitude of the responses, both decreases and increases. The polarity should be anodic, as it facilitates cortical depolarization. More details on MEP refer to Chap. 9. There is some controversy in the literature regarding the alarm signs for mMEP [11, 23] These criteria should not be evaluated in isolation, but together [11, 23–27]. Specifically for cervical surgeries, mMEP deterioration may be secondary to positioning alone, even if it occurs later. In these situations, the degree of cervical flexion/extension should always be reassessed, resulting in recovery of responses in most cases. Of note, in posterior approach for cervical kyphosis, improvement is commonly seen by reducing cervical flexion [20].  otor Evoked Potential: D-Wave (Note of the editors: this section translates M exclusively authors’ experience. It is not routinely included in commonsense protocols. Further evidences would be advisable) D-wave recording is done by placing an epidural catheter distally to the manipulated level (for monitoring), and another proximally placed catheter (sentinel) [21– 23]. The catheter must be placed by the surgeon himself, after the laminectomy. It can also be inserted percutaneously, like an epidural anesthesia; however, this option makes the process more invasive, and with greater risks, it is generally not recommended. D-wave was initially idealized for intramedullary spinal cord tumor surgeries (this theme is detailed in Chap. 28). However, because it is useful in the evaluation of pathologies that involve the first motor neuron, we extended its application to posterior cervical myelopathy surgeries, cervical or thoracic vertebral fractures and tumors, and thoracic disc herniations. The catheter must be placed over the spinal cord in the epidural space; for this reason, this test is restricted to spinal surgeries that extend to T9-T10 at the most. Transcranial electrical stimulation using a single stimulus results in D-wave (direct) and I-wave (indirect), the most important being the monosynaptic called “D-wave.” The stimulating electrodes can be placed at Cz/Cz + 6 cm as described in the original technique by Deletis et al. [21, 22]. However, to be able to observe side-­ to-­side amplitude discrepancies, which could not be visualized in the original technique, we suggest positioning the stimulating electrodes at C1/C2 or C3/C4. Traditionally, the D-wave alarm signal occurs if an amplitude deterioration greater than 50% occurs [22], indicating real motor pathway injury and poor neurological prognosis. However, in our clinical practice, we suggest a more conservative approach and earlier warning signs, in agreement with other authors [28, 29]. We alert the surgeon when there is a 20–30% decrement in D-wave amplitude, allowing reversibility maneuvers to be performed when possible. The main difficulties in performing D-Wave are: (1) surgeries that do not require laminectomy (e.g., endoscopic surgeries and cervical surgeries with anterior

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approach); (2) risks of percutaneous insertion of the epidural catheter; (3) unavailability of the specific epidural catheter. To overcome them, we developed a specific technique, with D-Wave recording with subdermal needles inserted into the interspinous ligaments of two adjacent vertebral spaces: D-Wave Interspinous Ligament Technique (DWILT) (Fig. 24.5). The stimulation parameters traditionally recommended for obtaining the D-wave were maintained (single pulse stimulus), since the stimulation with a train of multipulses could contaminate the D-wave responses (DWILT) with myogenic components of the paravertebral muscles (Fig. 24.6).

Somatosensory Evoked Potentials: SSEPs SSEPs will be recorded with corkscrew electrodes inserted at C3/C4 (upper limbs), Cz′/Fz (lower limbs), according to the 10/10 or 10/20 EEG system. Fractionating the sensory pathway, and adding recording electrodes, is suggested. For this purpose, additional sites are supraclavicular Erb’s point for upper limbs and popliteal fossa for lower limbs. They serve as a sentinel, proving the depolarization wave ascendency. More details on SSEP can be read in Chap. 8.

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Fig. 24.5  D-Wave Interspinous Ligament Technique – DWILT. (a) Subdermal straight twist needles inserted percutaneously. (b) Responses with D-wave bilaterally. (c) Subdermal needles inserted directly into the surgical field. (Editors’ note: Exclusively authors’ personal experience. Careful interpretation should be considered, since replication by other groups is recommended)

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Fig. 24.6  D-Wave Interspinous Ligament Technique – DWILT. D-Wave and Tc-MEP responses, both with multipulse train stimulus technique. Red squares: a patient with neuromuscular block (curarized). Green squares: a patient decurarized. (a) Red square: isolated D-wave responses; green square: D-wave responses with an overlap of myogenic components of the paravertebral musculature (multifidus). (b) Tc-MEP responses, to confirm the patient’s degree of curarization. (Note of the editors: DWILT corresponds exclusively to authors’ personal experience. Careful interpretation should be considered before adoption, since validation by other groups is highly recommended)

The stimuli to obtain SSEPs are performed on mixed peripheral nerves, pure sensory or corresponding dermatomes. The stimulation is done with supramaximal intensity, from 30 to 60 mA, frequency of 3.7 or 4.1 Hz and duration of 200 us/0.2 ms, preferably in the ulnar nerves (upper limbs) and tibial nerves (lower limbs). In upper limbs, it is also possible to use the median nerve, but our preference for the ulnar nerve is due to the following factors: (1) analysis of the complete posterior cervical spinal cord pathway, from C8-T1; (2) evaluation of upper limb positioning; and (3) better position of the electrodes medially at the wrist, leaving the lateral portion free for anesthetic procedures, such as puncture of the radial artery (Fig. 24.7). Continuous recording of SSEPs and mMEPs is difficult or even impossible during the entire surgical procedure. However, it is important to ask the surgeon to pause occasionally so that SSEPs and mMEPs can be checked. The goal is to avoid large gaps between two consecutive recordings and, during the opening phase, to update the baselines before the main surgical times. The recommended SSEP alarm signals are a 10% increase in latency and/or a reduction in amplitude greater than 50% [30]. The procedure should restart after a return of the potentials to at least 50% of baselines in less than 10 min. Changes that do not recover after 10 min are critical and may indicate posterior cord dysfunction. As highlighted for mMEP, altered SSEP responses in cervical spine surgeries may be secondary to positioning and this should be reevaluated.

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Anodo (+)

Catodo (-)

Fig. 24.7  Position of the electrodes on the wrist for SSEP stimulation – ulnar nerve. The electrodes are placed medially at the wrist, enabling the puncture of the radial artery in the lateral portion of the wrist

Electromyography: EMG EMG is the capture of the Motor Unit Action Potential (MUAP). The capture is done indirectly (involuntary) or directly (voluntary), through electrical stimulation, performed with the assistance of the surgical team. The patient cannot be curarized, which can be confirmed by TOF. EMG-fr EMG-fr is performed to detect spontaneous activity caused by mechanical stimulation or by neural dysfunctional discharges. The sources may be a dissection instrumental trauma or a compression or decompression maneuver. The neurophysiologist should carefully follow each step of the surgery to make the proper correlation of his tests with surgeon maneuvers. Inadequate alerts

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frequently derive from the following: (1) the neurophysiologist is not following the surgery step by step, or (2) he is using an incomplete protocol (“short protocol”), with recording electrodes in few myotomes. Both situations result in more risks than benefits to the patient. Neurotonic discharges should be communicated to the surgical team, as they alert to the proximity of neural tissue, and this can prevent the occurrence of injuries. The occurrence in multiple myotomes is possibility due to spinal cord percussion. Although we suggest the communication of every neurotonic discharge, the degree of insult to the neural tissue is mainly related to the constant presence of these discharges, during manipulation or persistent even after the surgeon has interrupted the maneuver. Neurotonic discharges may be present during manipulation of the dorsal column. In this situation, neurotonic discharges can arise from the reflex arc. Additionally, it is important to make the differential diagnosis with extracellular potassium deposition after neural tissue manipulation. For this purpose, the surgical field must be irrigated with warm serum, washing the extracellular potassium. If even after this maneuver the discharges remain, we consider a “true-positive” sign, and the probability of a neural insult must be considered. In this case, a control with mMEP must be performed, because depending on the degree of insult, this test may prove or discard the installation of motor impairment. It is worth emphasizing the difference in the analysis of neurotonic discharges in spinal surgeries, when compared to surgeries involving cranial nerves, especially the facial nerve. This is because, in spine surgeries, depolarization takes a longer and more complex pathway, starting in the first motor neuron, and following nerve roots, plexuses and, finally, differentiation into the various peripheral nerves, and its myotomes. Detailed analysis of neurotonic activity in cranial nerves is discussed in Chap. 21. Thus, we suggest that the alarm signals for EMG-fr are persistent neurotonic discharges during spinal and/or radicular surgical manipulation since the occurrence of these discharges in a severe form may be associated with reduced mMEP responses [30]. Also, neurotonic discharges can be visualized in all access routes in the cervical spine, including endoscopically (Fig. 24.8). EMG: Triggered (EMG-tg) The EMG-st is performed by the surgical team with the aid of a stimulator applied to the instruments, guides, and screws. The stimulation is performed by a monopolar electrode probe (cathode -) and a straight subdermal needle as (anode +). This technique is also useful for mapping neural structures in the operative field. As the stimulus is applied by the surgical team, not by the neurophysiologist, it is necessary to teach and guide the proper way to apply the stimulator (cathode) and position the reference needle (anode).

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Fig. 24.8  Examples of neurotonic discharges visualized in EMG-fr. (a) Neurophysiological monitoring during an endoscopic surgery. (b–e) Neurotonic discharges on the right upper limb, in the ascending order of intensity. (f) Presence of neurotonic discharges bilaterally

Discussion IONM During Cervical Spine Surgeries: Evidence IONM is indicated in several spinal surgeries with risk of iatrogenic injury and neurological deficit, like deformity correction surgeries and intramedullary tumors. In this context, cervical surgeries in all their approach routes have shown increasing benefits with IONM, due to their high risk of neural injury [24]. Multimodal monitoring with a combination of mMEP, SSEP, and EMG tests is currently recommended for all spine surgeries, including cervical, due to its higher sensitivity, and positive and negative predictive values [3, 31, 32]. IONM has evidence of high sensitivity and specificity for intraoperative detection of neurological injury during spinal approaches, as demonstrated by Fehlings et al. [35]. In addition, multimodal IONM can provide instant alerts to the surgical team in the occurrence of surgical insults [33–35]. Wiedemayer et al. [36] compared the rate of new neurological deficits between cases in which the surgeon reacted to an IONM alert and performed some intervention, versus those in which the surgeon did not react to the IONM alert. The authors concluded that IONM prevented the occurrence of postoperative deficit in 5.2% of the monitored cases. Similarly, Hilibrand et al. [33] described 12 patients with the loss of mMEPs responses, from whom 10 achieved complete reversal after the

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surgeon’s intervention and awoke without deficits. Conversely, the other 2 patients who had no improvement of MEP responses despite surgical intervention woke up with neurological deficits. Therefore, it highlights the correlation between the findings of improved mMEP in IONM, with the functional outcome of the patient. Thus, it is not uncommon to register neurophysiological alterations during the intraoperative period. Most of these alterations can be successfully reversed, either by modifying the technique employed by the surgical team or by temporarily stopping the surgery. Therefore, at the outcome perspective, the so-called “false positives” are actually “reversed true positives”; i.e., with the intervention performed still in the intraoperative period after the IONM alarm, new neurological deficits were avoided. Traditionally, the effectiveness of surgical decompression was proven by imaging studies (MRI changes) and postoperative clinical analysis of the patient. However, Wang et al. [32] stated that IONM has benefits in cervical decompression surgeries, not only to prevent nerve injury, but also to intraoperatively assure the surgical team that functional improvement has been achieved with the performed decompression. The authors concluded that intraoperative mMEP improvement is associated with better neurological and functional prognosis at the immediate and long-term follow-up. With regard to possible improvements in IONM responses, it should be analyzed in conjunction with variations in the anesthetic, hemodynamic, and clinical parameters (ruling out deep hypnosis, hypotension, anemia, hypovolemic shock, and hypothermia) since they directly interfere in IONM signals [37]. Yang et al. [38] observed that the IONM responses can increase up to 20% only with the increase of MAP, while Lyon et al. [39], in opposition, demonstrated the worsening of responses, usually insidiously, with the known phenomenon of anesthetic fade. Thus, effective decompression may not have immediate positive repercussions on neurophysiology if the above-mentioned parameters are inadequate. We suggest analyzing anesthetic and neurophysiological factors together, avoiding the occurrence of false-positive and false-negative results. In our clinical practice, we often observe significant improvement in IONM responses after decompression (Fig.  24.9), most commonly in cases of acute or subacute compression. These improvements are seen primarily in the SSEP absolute latencies and in an increase in mMEP amplitude and number of phases. To claim that the improvements are true and related to decompression, the mMEP and SSEP baseline must have been updated prior to this step. In agreement with other

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Fig. 24.9  Tc-MEP improved responses after decompression. (a) Tc-MEP responses baseline. (b) Tc-MEP increments after decompression

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authors [36], such improvements are usually seen earlier in mMEP and later in SSEP.  SSEP takes longer to respond to spinal decompression, assigning it a low sensitivity as a positive predictor [37, 38, 40]. One of the theories postulated for the correlation of improved IONM responses with surgical decompression, is vascular. Decompression favors increased arterial perfusion in neural tissue, generating improvement of installed ischemia and, consequently, improvement of mMEP responses [32, 33]. Another theory relates the improvement of responses to decompression of the neural tissue itself; that is, the immediate improvement of mMEP is related to enhanced neuronal excitability of the corticospinal tract [32, 33, 41].

C5 Palsy One of the most dread neurological complications in cervical surgeries is C5 palsy, which is an isolated deficit in the respective myotome after decompressive cervical surgeries. Although other roots are also at risk, this event occurs most commonly in the C5 root. Some etiologies have been proposed for this greater susceptibility [13, 14, 42, 43]: 1. The C5 root is shorter and its angle of exit from the brachial plexus is more obtuse than the others. Thus, it is more susceptible to direct injury during surgical maneuvers (including thermal injuries by drilling), preoperative positioning and over traction of the shoulders. 2. Because it emerges through the foramen between the C4/C5 level, the C5 root is usually in the central site of posterior multisegmental decompressive surgeries. Thus, when post-decompression spinal cord shift occurs, this root is more exposed to greater stress and greater perfusion/reperfusion changes. 3. The deltoid muscle is innervated almost exclusively by this root, which differentiates it from the other muscles of the upper limb. Thus, if a lesion of the C5 root occurs, the neurological deficit is more evident clinically. C5 palsy syndrome can occur in either the posterior (most common) or anterior approach. Wang et al. [13] performed a meta-analysis containing 61 studies and 725 patients with C5 palsy out of a total of 11,481 patients (6.3%). It was seen that the highest prevalence occurred in male patients, post laminectomy and fusion, and with ossification of the posterior longitudinal ligament. C5 paralyses are commonly considered late events, which would preclude their early detection and prevention by IONM [43]. However, in our practice, abrupt reduction in the amplitude of C5 mMEP responses is often observed in the decompression phase or a few minutes after decompression (Fig. 24.10). If this is detected by the IONM, the surgeon is notified immediately; and the most adopted strategy is to perform a C4/C5 foraminotomy [44].

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Fig. 24.10  Changes in the Tc-MEP of the left C5 root (deltoid muscle) during multilaminectomy in cervical surgery by posterior approach. Left responses of Tc-MEP (upper traces) and right responses of tc-MEP (bottom traces). (a) Left C5 responses present, immediately after multiple decompression – blue rectangle; (b) left C5 responses absent 14 min after decompression – red rectangle; (c) return of C5 responses to the left, 5  min after left C4/C5 foraminotomy  – blue rectangle

The White Cord Syndrome/Spinal Cord Reperfusion Injury In 2013, Chin and colleagues [45] described a rare complication after cervical decompression: the white cord syndrome. The term is related to the aspect found on MRI, with high-intensity intramedullary areas on T2-weighted magnetic resonance imaging. The main pathophysiological mechanism proposed for this injury was related to the reperfusion. The spinal cord impairment would occur after the reestablishment of normal blood flow in a previously compressed and hypoperfused or ischemic spinal cord tissue [45–47]. Therefore, another designation for this condition became Spinal Cord Reperfusion Injury. This syndrome is rare and describes the occurrence of neurological deficit in the postoperative period of an anterior or posterior decompressive cervical surgery in the absence of a determined cause for the deficit. It is important to emphasize that this syndrome should be considered a diagnosis of exclusion [45–49] and should only be established when all other causes of intraoperative and postoperative cord injury are ruled out. The clinical presentation varies in literature reports, with the occurrence of diplegia, quadriplegia, and hemiparesis, also with sensitivity changes [45–54]. Some authors reported clinical improvement in a few minutes [53], but most observed partial improvement of symptoms gradually, in weeks to months [45–54]. There is

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also a description of no clinical improvement at the follow-up, in a case related by Vinodh et al. [48]. The IONM findings in the reviewed cases were also diverse. In the cases reported in which the surgery was performed with IONM [45, 47, 50–54], there were cases with only alterations in SSEP, others with alterations in both mMEP and SSEP and one case without no alteration seen in the IONM [52]. The timing of the changes also varied: there was a case of sudden reduction in mMEP and SSEP after laminectomy, as well as changes that were only seen at the end of the surgery [47, 52]. Winginton et al. [53] report a case in which there was a transient drop in neurophysiological responses, with a return to baseline at the end of surgery. In this case, there was a correlation with the patient’s clinical status, who presented a transient neurological deficit in all four limbs, but with full recovery in a few minutes. In conclusion, white cord syndrome/spinal cord reperfusion injury is a rare condition, which can be catastrophic, with the possibility of quadriplegia in the outcome. IONM may or may not identify changes suggestive of this syndrome in the intraoperative period. For this reason, the neurophysiologist must be aware of this potential complication. Furthermore, it is emphasized that this syndrome is a diagnosis of exclusion, and it is always necessary to consider other more common causes for changes in neurophysiological responses or clinical neurological deficit.

Conclusion IONM has been proven to be useful in cervical surgeries, regardless of the approach chosen, anterior, posterior, open or endoscopic. One of the great challenges is the adequate neck positioning. The degree of head flexion or extension and shoulder traction aim to improve surgical field exposure for better surgeon’s visualization. This positioning may pose risk to the functionality of the nervous system, especially in patients with myelopathies. Thus, multimodal IONM is paramount to detect neural deterioration and to guide the repositioning. Additionally, multimodal IONM has also shown intraoperative benefits in detecting neural injury and eventually diagnosing the effectiveness of decompression. Finally, we emphasize that the evidence in favor of the use of multimodal IONM should not be evaluated considering solely the outcome, since surgeons’ interventional maneuvers after neurophysiologic alarm may prevent the occurrence of neurological lesions and their sequelae.

References 1. Beutler WJ, et al. Recurrent laryngeal nerve injury with anterior cervical spine surgery risk with laterality of surgical approach. Spine. 2001;26(12):1337–42. 2. Weinzierl MR, Reinacher P, Gilsbach JM, Rohde V.  Combined motor and somatosensory evoked potentials for intraoperative monitoring: intra-and postoperative data in a series of 69 operations. Neurosurg Rev. 2007;30:109–16.

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3. Akbari KK, et al. Do intraoperative neurophysiological changes during decompressive surgery for cervical myeloradiculopathy affect functional outcome? A prospective study. Global Spine J. 2020:2192568220951779. 4. Laratta JL, Há A, et  al. Neuromonitoring in spinal deformity surgery: a multimodality approach. Global Spine J. 2018;8:38–77. 5. Pajewski TN, Arlet V, Phillips LH. Current approach on spinal cord monitoring: the point of view of the neurologist, the anesthesiologist, and the spine surgeon. Eur Spine J. 2007;16(2):115–29. [cited 2007 Jul 10]. Available from: https://doi.org/10.1007/s00586-­007-­0419-­6. 6. Oglesby M, Fineberg SJ, Patel AA, Pelton MA, Singh K. Epidemiological trends in cervical spine surgery for degenerative disease between 2002 and 2009. Spine. 2013;38(14):1226–32. 7. Ibrahim T, et  al. The impact of neurophysiological intraoperative monitoring during spinal cord and spine surgery: a critical analysis of 121 cases. Cureus. 2017;9(11):e1861. PMID: 29375947. 8. Park JH, Hyum SJ. Intraoperative neurophysiological monitoring in spinal surgery. World J Clin Cases. 2015;3:765–7. 9. Marquez-Lara A, Nandyala SV, Hassanzadeh H, Noureldin M, Sankaranarayanan S, Singh K. Sentinel events in cervical spine surgery. Spine. 2014;39(9):715–20. 10. Ferreira RJR.  New bite block device: TONGARD®. Poster presentation in VI Simposio Latinoamericano de Monitorización Neurofisiológica Intraoperatoria. 2018. 11. Macdonald DB, Skinner S, Shils J, Yingling C, American Society of Neurophysiological Monitoring. Intraoperative motor evoked potential monitoring  – a position statement by the American Society of Neurophysiological Monitoring. Clin Neurophysiol. 2013;124(12):2291–316. https://doi.org/10.1016/j.clinph.2013.07.025. Epub 2013 Sep 18. PMID: 24055297. 12. Schwartz DM, et al. Neurophysiological identification of position-induced neurologic injury during anterior cervical spine surgery. J Clin Monit Comput. 2006;20(6):437–44. 13. Wang T, et al. Incidence of C5 nerve root palsy after cervical surgery: a meta-analysis for last decade. Medicine. 2017;96:45. 14. Currier B. Neurological complication of cervical spine surgery. C5 palsy and intraoperative monitoring. Spine. 2012;37:328–4. 15. Sadrolsadat S, Mahadavi A, et al. A prospective randomized trial comparing the thechnique of spinal and general anethesian for lumbar disc surgery: a study of 100 cases. Surg Neurol. 2009;71:60–5. 16. Menekse O. Sedation for percutaneous endoscopic lumbar discectomy, Sci. World J, vol. 2016, Article ID 8767410, 4 pages, 2016. https://doi.org/10.1155/2016/8767410. 17. Yeung AT. Lessons learned from 27 years’ experience and focus operating on symptomatic conditions of the spine under local anesthesia: the role and future of endoscopic spine surgery as a “disruptive technique” for evidenced based medicine. J Spine. 2018;7:413. 18. Ahn Y. Current techniques of endoscopic decompression in spine surgery. Ann Transl Med. 2009;7(Suppl 5):S169. 19. Sumiya S, Kawabata S, Ushio T, Sasaki J, Hashimoto T, Yoshii A, Okawa A. Verification by intraoperative spinal cord monitoring. Poster Session 2 Cervical spinal cord injury associated with neck flexion in posterior cervical decompression. J Neurol Sci. 2019;405S:104573. 20. Krzan M, Deletis V, Isgum V. Intraoperative neurophysiological mapping of dorsal columns. A new tool in the prevention of surgically induced sensory deficit? Electroencephalogr Clin Neurophysiol. 1997;2(102):37. 21. Deletis V. Intraoperative neurophysiology and methodologies used to monitor the functional integrity of the motor system. In: Neurophysiology in neurosurgery. Academic Press; 2002. p. 25–51. 22. Deletis V, Jay S.  Neurophysiology in neurosurgery: a modern intraoperative approach. Elsevier; 2002. 23. Kothbauer KF, Vedran D, Epstein FJ. Motor-evoked potential monitoring for intramedullary spinal cord tumor surgery: correlation of clinical and neurophysiological data in a series of 100 consecutive procedures. Neurosurg Focus. 1998;4(5):3.

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24. Langeloo DD, Journée HL, de Kleuver M, Grotenhuis JA. Criteria for transcranial electrical motor evoked potential monitoring during spinal deformity surgery a review and discussion of the literature. Neurophysiol Clin. 2007;37:431–9. 25. Calancie B, Harris W, Broton JG, et  al. “Threshold-level” multipulse transcranial electrical stimulation of motor cortex for intraoperative monitoring of spinal motor tracts: description of method and comparison to somatosensory evoked potential monitoring. J Neurosurg. 1998;88:457–70. 26. Quinones-Hinojosa A, Gulati M, Lyon R, et al. Spinal cord mapping as an adjunct for resection of intramedullary tumors: surgical technique with case illustrations. Neurosurgery. 2002;51:1199–206. discussion 1206–7. 27. Segura MJ, Talarico ME, Noel MA.  A multiparametric alarm criterion for motor evoked potential monitoring during spine deformity surgery. J Clin Neurophysiol. 2017;34(1):38–48. https://doi.org/10.1097/wnp.0000000000000323. PMID: 28045856. 28. Burke D, Richard GH.  Surgical monitoring of motor pathways. J Clin Neurophysiol. 1998;15(3):194–205. 29. Simon MV. Intraoperative neurophysiology: a comprehensive guide to monitoring and mapping. New York: Springer Publishing Company; 2018. 30. Nuwer MR, Dawson EG, Carlson LG, Kanim LE, Sherman JE. Somatosensory evoked potential spinal cord monitoring reduces neurologic deficits after scoliosis surgery: results of a large multicenter survey. Electroencephalogr Clin Neurophysiol. 1995;96:6–11. 31. Skinner SA, et  al. Electromyography detects mechanically-induced suprasegmental spi nal motor tract injury: review of decompression at spinal cord level. Clin Neurophysiol. 2009;120(4):754–64. 32. Wang S, et  al. Prognostic value of intraoperative MEP signal improvement during surgical treatment of cervical compressive myelopathy. Eur Spine J. 2016;25(6):1875–80. 33. Hilibrand A, et al. Comparison of transcranial electric motor and somatosensory evoked potential monitoring during cervical spine surgery. Spine J. 2003;3(5):73–4. 34. Hadley MN, et al. Guidelines for the use of electrophysiological monitoring for surgery of the human spinal column and spinal cord. Neurosurgery. 2017;81(5):713–32. 35. Fehlings MG, et al. The evidence for intraoperative neurophysiological monitoring in spine surgery: does it make a difference? Spine. 2010;35(9):37–46. 36. Wiedemayer H, et al. The impact of neurophysiological intraoperative monitoring on surgical decisions: a critical analysis of 423 cases. J Neurosurg. 2002;96(2):255–62. 37. Dulfer SE, et al. The influence of depth of anesthesia and blood pressure on muscle recorded motor evoked potentials in spinal surgery. A prospective observational study protocol. J Clin Monit Comput. 2021;35(5):967–77. 38. Yang J, et al. Raising mean arterial pressure alone restores 20% of intraoperative neuromonitoring losses. Spine. 2018;43(13):890–4. 39. Lyon R, et al. Progressive suppression of motor evoked potentials during general anesthesia: the phenomenon of anesthetic fade. J Neurosurg Anesthesiol. 2005;17(1):13–9. 40. Schwartz DM, et  al. Neurophysiological detection of impending spinal cord injury during scoliosis surgery. JBJS. 2007;89(11):2440–9. 41. Deletis V, Sala F. Intraoperative neurophysiological monitoring of the spinal cord during spinal cord and spine surgery: a review focus on the corticospinal tracts. Clin Neurophysiol. 2008;119(2):248–64. 42. Yonenobu K, et al. Neurologic complications of surgery for cervical compression myelopathy. Spine. 1991;16(11):1277–82. 43. Shinomiya K, et al. Morphology of C5 ventral nerve rootlets as part of dissociated motor loss of deltoid muscle. Spine. 1994;19(22):2501–4. 44. Thompson SE, et al. C5 palsy after cervical spine surgery: a multicenter retrospective review of 59 cases. Global Spine J. 2017;7(1):64–70.

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45. Chin KR, Seale J, Cumming V. “White cord syndrome” of acute tetraplegia after anterior cervical decompression and fusion for chronic spinal cord compression: a case report. Case Rep Orthop. 2013;2013:697918. 46. Epstein NE. Reperfusion injury (RPI)/white cord syndrome (WCS) due to cervical spine surgery: a diagnosis of exclusion. Surg Neurol Int. 2020;11:320. 47. Mathkour M, et al. Reperfusion “white cord” syndrome in cervical spondylotic myelopathy: does mean arterial pressure goal make a difference? Additional case and literature review. World Neurosurg. 2020;137:194–9. 48. Vinodh VP, et al. White cord syndrome: a devastating complication of spinal decompression surgery. Surg Neurol Int. 2018;9:136. 49. Acharya S, et  al. Misdiagnosis of “white cord syndrome” following posterior cervical surgery for ossification of the posterior longitudinal ligament: a case report. Surg Neurol Int. 2021;12:244. 50. Giammalva GR, Maugeri R, Graziano F, et  al. White cord syndrome after non-contiguous double-level anterior cervical decompression and fusion (ACDF): a “no reflow phenomenon”. Interdiscip Neurosurg. 2017;7:47–9. 51. Papaioannou I, Repantis T, Baikousis A, Korovessis P. Late-onset “white cord syndrome” in an elderly patient after posterior cervical decompression and fusion: a case report. Spinal Cord Ser Cases. 2019;5:28. 52. Antwi P, Grant R, Kuzmik G, Abbed K. “White cord syndrome” of acute hemiparesis after posterior cervical decompression and fusion for chronic cervical stenosis. World Neurosurg. 2018;113:33–6. 53. Wiginton IVJG, Brazdzionis J, Mohrdar C, Sweiss R, Lawandy S.  Spinal cord reperfusion injury: case report, review of the literature, and future treatment strategies. Cureus. 2019;11:5279. 54. Busack CD, Eagleton BE. White cord syndrome causing transient tetraplegia after posterior decompression and fusion. Ochsner J. 2020;20(3):334–8.

Chapter 25

Tethered Cord Syndrome Vanise Campos Gomes Amaral, Sérgio Cavalheiro, Ricardo José Rodriguez Ferreira, and Maria Lucia Furtado de Mendonça

Abbreviations BCR Bulbocavernosus reflex CMAP Compound motor action potential CSF Cerebrospinal fluid EEG Electroencephalography EMG Electromyography fEMG Free-running spontaneous EMG H reflex Hoffman reflex IONM Intraoperative neurophysiological monitoring MEP Motor evoked potential MRI Magnetic resonance imaging SSEPs Somatosensory evoked potentials TCS Tethered cord syndrome V. C. G. Amaral (*) Universidade do Estado do Amazonas/Escola Superior de Ciências da Saúde-UEA/ESA, Manaus, AM, Brazil S. Cavalheiro Department of Neurosurgery, Universidade Federal de São Paulo, São Paulo, SP, Brazil R. J. R. Ferreira AACD - Disabled Child Care Association, São Paulo, SP, Brazil Dr Ricardo Ferreira Clinic, São Paulo, SP, Brazil Spine Surgery Department at Orthopedics and Trauma Institute of Clinical Hospital of the University of São Paulo Medical School, São Paulo, SP, Brazil M. L. F. de Mendonça Clinical Neurology and Neurophysiology, Intraoperative and Critical Care Clinical Neurophysiology, Neuro Logical Clinica Médica, Rio de Janeiro, RJ, Brazil © The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 S. M. Verst et al. (eds.), Intraoperative Monitoring, https://doi.org/10.1007/978-3-030-95730-8_25

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Triggered EMG Transcranial electrical stimulation Tethered spinal cord

Introduction Tethered cord syndrome is characterized by the inability to move the spinal cord during the different stages of life. Clinically, the syndrome is associated with a progressive neurological, orthopedic, and urological deterioration and misplacement of the conus medullaris. These symptoms can occur alone or in combination. Recently, the term “occult tethered cord” has been used to characterize a syndrome with classic symptoms of tethered cord syndrome (TCS) but with conus medullaris in the normal position and often associated with a thickened filum terminale [1]. Although the term is restricted to the spinal cord, some patients present anchoring of the brainstem, which must be considered under the same principles, especially when lesions affect the medulla oblongata [2, 3]. Anatomically, the spinal cord occupies the entire spinal canal during the fetal stage. At birth, the conus medullaris is at the T12–L1 or L1–L2 level, in most cases. Misplacement of the conus medullaris can indicate a tethered spinal cord. The congenital diseases that are most frequently associated with a tethered spinal cord are open and occult spinal dysraphisms. The best example of open spinal dysraphism is myelomeningocele (Fig. 25.1), while examples of occult spinal dysraphism include lipomeningocele, diastematomyelia, filum terminale lipomas, mangrove myelomeningocele, myelocystocele, and dermal sinus (Fig.  25.2). The acquired diseases that can occur with a tethered spinal cord include postoperative intramedullary tumors, fibrotic scarring after spinal cord injuries, and sequelae of meningitis, but these are rare. a

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Fig. 25.1  Open spinal dysraphisms: Myelomeningocele. Panel (a) shows myelomeningocele intrauterine. Panel (b): Myelomeningocele surgery in the first 6 h of life. Panel (c): Myelomeningocele with transillumination

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Fig. 25.2  Occult spinal dysraphisms. Panel (a): Lipomeningocele. The lumbar lesion is often covered with skin, and there is never hydrocephalus or herniation of the cerebellar tonsils. Panel (b): Sinus dermal with hemangioma. Panel (c): Gluteal fold asymmetry. Panel (d): Sacral skin appendages. Diastematomyelia, dermal sinus, and filum terminale lipomas can cause a TCS and are very difficult to diagnose prenatally. It should be suspected at birth based on cutaneous stigmas, such as hemangiomas, sacral dimples, sacral skin appendages, and gluteal fold asymmetry

The spinal cord is not able to return to its normal position in congenital diseases that cause a tethered spinal cord and are treated during the fetal stage or the first months of life. Therefore, the position of the conus medullaris does not change in the magnetic resonance imaging (MRI) scans of patients after the correction of myelomeningocele or lipomeningocele. Furthermore, there is always a radiological diagnosis of tethered spinal cord that, clinically, is not real. The diagnosis of TCS related to the follow-up of spinal dysraphism is a clinical diagnosis, and not a radiological diagnosis, based on a progressive worsening of symptoms, with pain in the lumbar region or at the level of the lesion that is associated with neurological, orthopedic, or urological worsening. Therefore, it is very important for the patient to have continuous and individualized follow-up.

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The scope of this chapter is to provide the reader with an overview of the clinical evaluation and surgical techniques for correction of a tethered spinal cord, from the view of a neurosurgeon, and to describe the main intraoperative neurophysiological monitoring (IONM) techniques used in these procedures, from the view of a neurophysiologist.

View of the Neurosurgeon Clinical Evaluation Both open and occult spinal dysraphisms have a high incidence of tethered spinal cord from the fetal stage. The earlier the spinal cord is released, the better the prognosis. Open spinal dysraphism is the most important example of myelomeningocele and can be corrected during the fetal stage or shortly after birth. However, occult spinal dysraphisms, such as lipomeningocele, diastematomyelia, dermal sinus, and filum terminale lipomas, in our experience, have a better outcome when corrected after 6 months of life. In cases of occult tethered spinal cord, the diagnosis can be made very late and is most often associated with sphincter disorders. Immediate treatment can significantly improve symptoms. Therefore, each pathology should have a precise diagnosis and individualized follow-up.

Prenatal Evaluation Myelomeningocele is the most frequent type of open spinal dysraphism, with an incidence of 1:1000 live births. Diagnosis during the fetal stage has become more common with routine prenatal ultrasound. In addition to spinal alterations, with neural tissue herniation due to dysraphism, there are cranial alterations characteristic of this malformation. The lemon sign, characterized by flattening of the frontal bones, and the banana sign, characterized by an inversion of the curvature of the cerebellum, are found in more than 90% of cases. These signs are caused by an intracranial hypotension, the so-called dry brain, as a consequence of the fistula and loss of cerebrospinal fluid (CSF) into the amniotic cavity. Due to herniation of the cerebellum through the foramen magnum, there can be varying degrees of hydrocephalus. It is also possible to assess the degree of herniation of the cerebellar tonsils, the so-called Chiari type II, with ultrasound (Fig. 25.3). An examination of the lower limbs can be used to assess motor abnormalities. The presence of clubfeet or dislocation of the femurs is indicative of poor motor prognosis, and leg and thigh circumference measurements and the replacement of muscle mass by fat can provide a prognosis, even during the fetal stage [4]. The goal of fetal surgery for myelomeningocele is to prevent hydrocephalus, which is obtained in 50% of patients, according to MOMS [5].

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Fig. 25.3  Diagnosis of spinal dysraphisms during fetal stage. Panel (a) shows the lemon sign, characterized by flattening of the frontal bones. Panel (b) banana sign, characterized by an inversion of the curvature of the cerebellum, is found in more than 90% of cases. Panel (c): Myelomeningocele, in operation room. Panel (d): Myelomeningocele Intrauterine. Panel (e): Myelomeningocele intrauterine with Chiari Tipo II

Lipomeningocele is a occult spinal dysraphism and should be well distinguished from myelomeningocele. The lumbar lesion is often covered with skin, and there is never hydrocephalus or herniation of the cerebellar tonsils. Lower limb motor changes, such as clubfoot, can be identified. There is no need to correct an intrauterine lipomeningocele since the neural tissue is protected by skin and there is no risk of hydrocephalus. Diastematomyelia, dermal sinus, and filum terminale lipomas are other types of spinal dysraphisms that can cause a tethered spinal cord, are very difficult to diagnose prenatally, and should be suspected at birth based on cutaneous stigmas, such as hemangiomas, sacral dimples, sacral skin appendages, and gluteal fold asymmetry (Fig. 25.2).

Surgical Treatment During the Fetal Stage The intrauterine treatment of myelomeningocele has a level of evidence 1A and should be performed before 27 weeks of gestation. Early surgery reduces the onset of hydrocephalus and improves motor deficits, as demonstrated by the MOMS [5]. The occipital bone is composed of several small bones that fuse at approximately 27 weeks of gestation. An intracranial hypotension, characteristic of myelomeningocele, that is caused by the fistula and CSF leak accelerates this ossification and produces a small posterior fossa that is unable to accommodate the cerebellum. This leads to herniation of the cerebellar tonsils and biventricular lobules through the foramen magnum, which compresses the brainstem and cerebral aqueduct and causes an obstructive hydrocephalus. Surgery performed before 27  weeks of

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gestation restores CSF circulation, thereby increasing intracranial pressure and thus, the posterior fossa, reducing herniation of the cerebellum and its compression against the cerebral aqueduct. Early protection of the neural tissue herniated by spinal dysraphism prevents its deterioration due to intrauterine trauma and exposure to amniotic fluid, which becomes more acidic as the pregnancy progresses. Therefore, a gestational age of 19–27 weeks is ideal for performing the intrauterine procedure. The fetal surgery for myelomeningocele correction can be performed using two approaches: open, as proposed by the MOMS, and endoscopic. The endoscopic surgery is still in its experimental phase. Procedures that only cover the wound with dura mater substitutes should be avoided, as they do not release the spinal cord. A ligament that attaches the spinal cord to the apical part of the dysraphism has been found during surgery and should be cut to release the spinal cord. In our case series of 1000 surgeries, performing the surgery during the fetal stage led to a tenfold decrease of the risk of a tethered spinal cord. Closed spinal dysraphisms are not indicated for surgery during the fetal stage as they do not present a risk of hydrocephalus or deterioration for amniotic fluid exposure. For patients with closed spinal dysraphisms, surgery is indicated over the age of 6 months, since this enables a more precise surgery with IONM.

Postnatal Surgical Treatment Open Spinal Dysraphism Since myelomeningocele is an open spinal dysraphism, the surgical procedure should be performed as early as possible. Thus, we have operated on most of our patients within their first 6 h of life (Fig. 25.1). At this stage, the surgeon should keep in mind that it is not enough to just cover the dysraphism; the spinal cord must be released. A wide dissection of the placode with release of the roots and all adhesions must be performed. All layers must be closed, namely, the placode, dura mater, aponeurosis, subcutaneous cellular tissue, and skin. In cases of rachischisis, the lesions are often extensive, but the nervous tissue is preserved, and the neurological prognosis is usually excellent. This differs from patients with large myelomeningoceles, in which the roots may adhere to the herniated dural sac and neurological deficits may be severe. IONM in these newborns still needs to be better defined, since the obtained potentials are erratic and may not help clinicians intraoperatively. The placode, which should have a cylindrical shape, is usually flattened. The dissection should be precise so that no skin fragment remains and there is no subsequent development of an epidermoid tumor that will cause a retethered spinal cord. The reconstruction of its normal anatomical shape can be attempted, without worsening the neurological deficit. Therefore, sutures that taper the placode edges can be employed, preferably using 6.0 or 7.0 absorbable sutures, or even fixation with fibrin glue. The dura mater must be

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hermetically closed to avoid a fistula and CSF leaks. Nonabsorbable sutures should be used, and we prefer the Prolene 5.0 suture, with a vascular needle. We do not use dura mater sealants at this age. We always close the aponeurosis with an absorbable Monocryl 4.0 or 5.0 suture. In the skin, we use simple and separate sutures with a nylon 6.0 suture. When the skin is closed, it is important to make sure that the skin is not under tension, and, if it is, we prefer to perform a myocutaneous flap in the form of a “Yin-Yang” Z-plasty. In cases of severe kyphosis, we correct the bone defect with the same procedure, to have a tension-free skin suture. Occult Spinal Dysraphism The occult spinal dysraphisms are usually corrected around 6 months of age. There are several reasons for selecting this age: (1) the child does not walk yet, so even if the spinal cord is tethered, it will not cause any deficit for the patient; (2) the newborn’s physiological anemia has disappeared; (3) the coagulation cascade is well developed. At this stage, all dysraphisms are operated on with the aid of a surgical microscope, an ultrasonic aspirator, and IONM. Each type of dysraphism is treated with a distinct surgical technique. The dermal sinus must be completely resected, to prevent the appearance of spinal abscesses and to release the spinal cord. As for diastematomyelia, the intramedullary bone beam must be removed and the dura hermetically closed. Lipomeningocele is the most frequent closed spinal dysraphism and can be classified into four types: dorsal, transitional, chaotic, and terminal [6]. In this type of injury, the surgical procedure is contraindicated without IONM (Fig. 25.4). A thorough neurological evaluation should be performed in association with urological and orthopedic evaluations. We often find asymmetries in the feet and sometimes in the leg. Such alterations are irreversible, even with surgical treatment, and can be attributed to surgery if not checked preoperatively. The preservation of the last sacral roots is essential for the sphincter and erectile functions. Removal of an intramedullary lipoma with increased postoperative neurological deficit is not justified. On the other hand, a close relationship between the neurophysiologist and the neurosurgeon is very important, to ensure that everyone has a common language. We should respect the neurophysiologist and stop the procedure by mutual agreement, keeping in mind that the main goal is to reduce postoperative neurological deficits.

Surgical Treatment of Spinal Cord Retethering We use the term retethering to refer to the second surgical approach, as these are always new procedures after treating dysraphic pathologies. The treatment of a retethered spinal cord is a neurosurgical challenge, as nerve tissues are damaged,

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Fig. 25.4  Tethered spine cord (TSC) associated to lipomeningocele. Panel (a): Surgery indicated in a 6-month-old boy. Multimodal IONM technique. Panel (b): Preoperative sagittal MRI scan with TSC showing closed spinal dysraphisms (lipomeningocele). Panel (c): Sample obtained during surgery shows stable posterior tibial SSEPs bilaterally as well as f EMG and MEPs from abductor pollicis brevis (as a technique control), iliopsoas, quadriceps femoris, tibialis anterior, gastrocnemius medial, abductor hallucis, and anal sphincter. Panel (d) shows stable bilateral BCR with latencies of 451 ms (left) and 415 ms (right)

sometimes to the limit of their resistance. A more aggressive procedure can cause irreversible damage. In these cases, in addition to a clinical evaluation and imaging exams, lower limb somatosensory evoked potentials (SSEPs) can be indicators of a tethered spinal cord, especially in walking patients with a lesion below L4 [7, 8]. The frequency of tethered spinal cord in cases of myelomeningoceles operated on after birth ranges from 14% to 19% [9–11]. Our series showed retethering in 15% of the patients who underwent operations for myelomeningocele. Clinically, pain was the most common complaint (90% of the cases). Neurological worsening was observed in 30% of the cases and worsening of the urological disorder in 20%. The upper limb evaluations detected fine motor deficits in 5% of the cases, which were aggravated by the presence of hydrocephalus. Therefore, evaluation of the upper limbs should be part of the propaedeutics of patients with open and closed spinal dysraphisms and can assist in the diagnosis of a tethered spinal cord [12]. From a radiological point of view, the most common alteration was scoliosis, followed by worsening of sacral kyphosis. The identification of an epidermoid tumor was the most frequent indication of surgery, followed by syringomyelia. The surgical treatment showed resolution of pain in 98% of cases and of sphincter disorders in 88% [13–15].

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The surgical microscope is first used for the skin incision. In many centers that perform endoscopic surgeries to correct myelomeningocele during the fetal stage, the placode adheres to the subcutaneous tissue, and we can inadvertently cut a root during the skin incision. The neurophysiologist must pay attention to the incision. It is common to find patients with complete sphincter dysfunction and functional sacral S2, S3, and S4 roots upon testing, and we are not comfortable cutting them. Two structures should be identified, namely, the apical ligament that attaches the dura mater in its midline to the spinal and filum terminale. It is simple to cut the apical ligament, but we can inadvertently open the dura mater in a region superior to the previous dura mater opening. Care should be taken when cutting the filum terminale, as the S4 roots are usually attached to it, and it is important to clot the filum terminale artery before cutting it, to prevent bleeding. In the first procedure, we should always opt for techniques that prevent spinal cord retethering, although there is no consensus in the literature on prevention methods. Pang et al. proposed the use of dural grafts to increase the dural canal radius and prevent retethering, especially in cases of lipomeningocele [16], while Walker et al. [17] proposed amniotic membrane grafting to prevent spinal cord anchoring at the dura mater suture. The surgical treatment of a retethered spinal cord should be accepted as a possibility for neurological improvement and should always be indicated by a multidisciplinary team.

View of the Neurophysiologist I ntraoperative Neurophysiologic Monitoring in Tethered Cord Syndrome (TCS) IONM in cases of tethered cord syndrome is always a challenge for the neurophysiologist, particularly in cases associated with lipoma and/or spinal cord retethering. The main objectives of IONM are to use mapping techniques to identify ambiguous and viable neural tissues and assess the functional integrity of motor and somatosensory pathways and reflex circuits, such as the bulbocavernosus reflex (BCR) and the Hoffman reflex (H reflex). The protocol selected for monitoring these cases should be efficient and sufficient to minimize postoperative neurological deficits.

Multimodal Protocols for TCS Surgery The TCS protocols should be multimodal and designed according to the neurological condition of each patient. The suggested multimodal approach for TCS includes free and stimulated electromyography (EMG), motor evoked potential (MEP),

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Fig. 25.5  TSC associated to a lipoma. Panel (a): Preoperative sagittal T2 weight MRI scan demonstrated TSC, lipoma, and syringomyelia in a 5-year-old boy with gait dysfunction and asymmetries in the feet. Panel (b): Abnormal f EMG discharges recorded during resection of the lipoma. Right panel (red color) shows neurotonic discharge in right tibialis anterior, peroneus longus, and gastrocnemius medial; bilateral discharges (mechanical irritation of motor fibers) in left (blue panel) and right abductor hallucis and left anal sphincter. Stable bilateral BCR is marked with a red arrow

lower limb somatosensory evoked potentials (SSEPs), pudendal nerve SSEP, BCR, H reflex, and electroencephalography (EEG) (Fig. 25.4). Of all these modalities, mapping techniques (triggered EMG) play an important role, since they are essential for differentiating functional neural structures that must be preserved from nonfunctional vestigial roots or fibrous bands that can be cut to release the spinal cord. However, monitoring the other modalities during surgery helps to minimize the risk of unfavorable postoperative outcomes. This chapter does not intend to discuss IONM techniques in detail. We discuss the most relevant aspects in TCS surgeries. For more details about SSEP, MEP, and EMG, please refer to Chaps. 8, 9, and 11, respectively.

Electromyography (EMG) Two types of EMG are monitored in TCS surgeries: free-running spontaneous EMG (fEMG) and triggered EMG (tEMG). Free-Running Spontaneous EMG (fEMG) The roots of L2 to S4 are continuously monitored by fEMG to detect normal and abnormal muscle activity (Figs. 25.5 and 25.6).

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a

b

Fig. 25.6  Abnormal f EMG discharges recording during resection of retethered spinal cord by a lipoma. The treatment of a retethered spinal cord is a neurosurgical and neurophysiologist challenge, as nerve tissues are damaged, sometimes to the limit of their resistance. Panel (a): Left side (blue color) shows mechanical irritation of motor fibers, duration resection of lipoma, in tibialis anterior, abductor hallucis, and gastrocnemius medial; Panel (b): Right side (red color) shows mechanical irritation of motor fibers, duration resection of lipoma, in tibialis anterior, abductor hallucis, and gastrocnemius medial muscle

Several types of electrodes can be used to record muscle activity, but subdermal needle electrodes are used more frequently. Bipolar recording is carried out with a pair of needle electrodes inserted transcutaneously into the motor area of each selected muscle. Our protocol includes bilateral muscle recordings from abductor pollicis brevis (as control), iliopsoas, quadriceps, tibialis anterior, medial gastrocnemius, peroneus longus, abductor hallucis, and anal sphincter (Table 25.1). During TSC approach, due to an increased risk of damaging the motor roots of the bowel and bladder, it is essential to monitor the anal and urethral sphincter muscles [18, 19]. Other muscles can also be used if necessary. The following settings are used: a time window from 100 to 200 ms/div. Low-­ frequency filters and high-frequency filters are set between 10 Hz and 2–5 kHz [20]. The appropriate sensitivity settings are 50  uV to 2  mV, which can be adjusted according to the amplitude of the recorded muscle activity.

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Table 25.1  Muscles commonly used in IONM in TCS Muscle Iliopsoas Quadriceps femoris Tibialis anterior Peroneus longus Gastrocnemius (lateral or median heads) Abductor hallucis Anal sphincter

Roots L2–L3–L4 L2–L3–L4 L4–L5 L5–S1–S2 S1–S2 S1–S2 S2–S3–S4

Neurotonic discharges are spontaneous potentials that occur in response to mechanical, thermal, or metabolic irritation of the ventral root. The surgeon should be alerted in order to prevent neural damage. Important aspects should be taken into account to avoid misinterpreting fEMG. Usually, cases of sudden nerve transection or vascular injury may not originate neurotonic activity. Moreover, mechanical activation of the distal stump of a sectioned nerve can also produce EMG activity in the corresponding muscle, thus giving the false impression that the injured nerve is still intact. Conversely, a previously damaged motor root can express decreased excitability and, therefore, low probability of presenting neurotonic activity due to mechanical manipulation. In order not to alert the surgeon unnecessarily, the spontaneous motor unit discharges that occur in cases of “light anesthesia” should be distinguished from abnormal discharges. During “light anesthesia,” motor unit potentials (from several different myotomes) may fire randomly, while stressful events are commonly more focused in the myotome under irritation. The irritative activity on the fEMG has a high degree of sensitivity to predict new deficits but a low degree of specificity [21]. Gunnarsson et  al. [22] showed that neurotonic discharges are frequent in certain spinal surgeries but that they do not always signalize nerve root damage. Robust criteria for interpreting fEMG changes during TCS surgery still need to be defined. Triggered EMG (tEMG) for Motor Root Mapping Triggered EMG is a reliable method for identifying functional neural tissue [23]. The surgeon performs direct electrical stimulation on the structures of interest with a handheld probe stimulator, to identify motor nerve roots and distinguish them from fibrous tissue. The resulting compound motor action potential (CMAP) is recorded in the muscles of the lower limbs, anal sphincters, and, if possible, urethral sphincters [24, 25]. We use bipolar stimulation, which allows a more focal current distribution. Monopolar stimulation results in a general current spread in the surgical field. When the anatomy is very distorted, we start with monopolar stimulation to find nerve structures within the tissue and then shift to bipolar stimulation, for a more precise

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location. In very young children, a small concentric bipolar stimulator may be used, as double-tip bipolar stimulator can cause significant current spread in this age group. Sala et al. [26] suggest a protocol using (1) constant current with a pulse duration of 200 μs, slowly increasing the intensity from of 0.01 mA up to 3 mA, at 1 Hz frequency until a CMAP response is elicited, (2) sensitivity settings of 50 uV, (3) filters and muscle recordings as already described in section “Free-Running Spontaneous EMG (fEMG)”, and (4) time window of 5 ms/division. Unlike them, we use a shorter pulse duration of 100 μs because the threshold for evoking a CMAP of a normal motor root is about 0.2–1.0 mA. Sensory roots require a higher stimulus intensity, of approximately 1.0–2.0  mA, with the same pulse duration. Shorter charges reduce electrical spread (Figs. 25.7, 25.8, and 25.9). De Almeida et al. [27] suggest that for young children, due to lack of complete myelin development, a higher threshold may be necessary. Conversely, young children’s ventral roots are generally of smaller diameters than adults’, thus the stimulation threshold can be lower, ranging between 0.5 and 1.5 mA, for a pulse duration of 200 μs. Husain et al. [28] describe that a voltage intensity up to 1 V (in children) and up to 7 V (in adults) is needed to generate a response from nerve roots. Kothbauer et al. [29] suggested that normal nerve roots often require less than 1 V for activation, whereas spinal cord stimulation usually requires about 10 V. There are two possibilities in cases of no CMAP response after stimulation. Assuming that the stimulation and anesthesia parameters are adequate, either the stimulus intensity is below the threshold, or the stimulated structure is not a motor root. For better checking it out, the stimulus intensity should be gradually increased a

b

c

d

Fig. 25.7  TSC in a 6-month-old boy. Panel (a): Preoperative sagittal T2 weight MRI scan demonstrate TSC associated with sinus dermal and filum terminale lipoma. Panel (b): Multimodal IONM monitoring in closed spinal dysraphisms with cutaneous stigmas. Panel (c): T-EMG – using bipolar handheld stimulator: CMAPs recorded in left L5 (peroneus longus and anterior tibialis) and spread for S1 and anal sphincter with 1.3 mA (0.1 ms duration). Panel (d): After reduction the stimulus intensity for 1.0 mA the CMAP: selective recordings at L5 muscles. The lack of response in the abductor hallucis corroborates the selectivity L5 stimulation

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b

c

Fig. 25.8  Panel (a): Preoperative sagittal T2 weight MRI scan demonstrate TSC associated with lipomeningocele. Panel (b): T-EMG using bipolar handheld stimulator elicits CMAPs bilaterally with 1.3 mA (0.1 ms): spread of stimulus through cauda equina at the beginning of the procedure. Bilateral response is also seen with placode stimulation. Panel (c): T-EMG, performed during separation of roots from placode, showed CMAPs in the most proximal muscle (iliopsoas and quadriceps) at the right side (red)

a

b

c

Fig. 25.9  Panel (a): TSC and filum terminale lipoma. Panel (b): T-EMG – Stimulation with bipolar handheld stimulator triggers CMAPs in left side (blue) in peroneus longus, anterior tibialis, abductor hallucis, and gastrocnemius medial muscle. Panel (c): T-EMG – Stimulation with bipolar handheld stimulator triggers CMAPs in right side (red) in peroneus longus, anterior tibialis, abductor hallucis, and gastrocnemius medial muscle

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up to 6 mA (100 μs), which should elicit a response from a normal motor root. Thus, a nonresponsive structure at 6 mA can be taken as nonneural and be sacrificed. The identified stimulus threshold can be further used to distinguish functional neural structures that should be preserved from nonfunctional vestigial roots or fibrous bands that can be cut to release the spinal cord. Yet, the presence of injured motor roots may require a higher stimulation threshold. The surgeon must understand the importance of threshold stimulation. Increasing the stimulus intensity above the threshold can spread the current and thus reduce specificity. The threshold has additional prognostic value, as it can predict the postoperative outcome. The motor roots are stimulated at the same location and with the same stimulus intensity, before and after spinal cord/roots release. If there is no injury during the resection process, the final-to-baseline CMAPs threshold keeps even. However, damage during manipulation can be due to stretching, partial section, and ischemic events, resulting in higher final threshold. It may indicate postoperative worsening of the neurological function. Similarly, a lower threshold after release usually represents a better prognosis [30]. Stimulation of single motor roots is difficult, as the roots are usually clustered, and the surgical field is relatively small. Therefore, most elicited responses are often in all muscles on the left or right side (Fig. 25.9b, c). If the response is bilateral, a current spread has most likely occurred, and the stimulus intensity should be reduced. Stimulation of the placode will also evoke bilateral responses (Fig. 25.8b). For more selective responses in the sacral roots, it is ideal to stimulate more distally, with the assumption that more proximal lumbar roots have already left the spinal canal. Furthermore, as the goal of tEMG is to identify all nerve roots for additional protection, eliciting individualized CMAPs is not fundamental. Regarding stimulation of the filum terminale (which generally has no neural elements), we believe that a maximum current intensity of 10 mA and 100 us of pulse duration is sufficient in most cases. If CMAPs is not elicited at this intensity, we recommend cutting the filum. Yet, Quiñones-Hinojosa et al. [31] advocate that safe identification of the filum terminale may require stimulus intensities much higher than threshold (up to 100 V). It must be pinpointed that stimulation of the filum terminale even at a low intensity (at the range used to evoke CMAPs of normal ventral roots) can evoke a motor response. Positive mapping warrants further investigation, as filum terminale stimulation should not evoke CMAPs. In this case, the surgeon should inspect its ventral aspect since a small root can be adhered to it, usually S4. After separating the root, the stimulation should be repeated, to ensure that no other roots are attached to the filum terminale. If no CMAP is evoked, the filum can be safely cut (Fig. 25.10). Caution should be taken during stimulation, as current spread through the CSF or meninges can be a confounding factor and trigger muscle responses in nonfunctional structures. The surgeon should ensure to have a dry surgical field and that the stimulator probe is selectively placed, and not in contact with adjacent nerve roots. In TCS, safely sectioning fibrous bands or nonfunctional radicles or rootlets has a significant impact on the degree of spinal cord release, and IONM is critical for optimizing surgical outcomes.

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b

c

Fig. 25.10  Stimulation of the filum terminale at a low intensity (at the range used to evoked CMAPs of normal ventral roots) can evoke a response. Positive mapping warrants further investigation, as filum terminale stimulation should not evoke CMAPs. Panel (a): Shows the filum terminale. Panel (b): Surgeon inspect the ventral aspect the filum and found a small, adhered root, usually S4. Panel (c): After separating the root, the stimulation should be repeated, to ensure that no other roots are attached to the filum. If no CMAP is evoked, the filum terminale can be safely cut

Motor Evoked Potential The functional integrity of motoneurons is assessed by activating the motor cortex by transcranial electrical stimulation (TES). The electrodes that are preferably used during this procedure are corkscrew electrodes. They have low impedance and provide a more reliable fixation to the patient’s scalp. Some centers choose to use subdermal needle electrodes especially for small children. Great care must be taken in newborns and children who still have open fontanels and in those with a ventriculoperitoneal shunt so that the electrode does not penetrate the fontanel or valve/ shunt. EEG electrodes should be preferred in these patients [32]. Lieberman [33] showed that TES motor thresholds are negatively correlated with age, with a higher threshold in younger children, considering other stimulus variables to be even (pulse duration and interstimulus interval). The selection of the site for placing the stimulating electrodes is crucial for obtaining MEPs with maximum amplitude, using the lowest possible intensity, aiming to reduce patient’s movements. Therefore, we suggest the following sites: C4, C3, C1, and C2, with C1 and C2 situated midway between C3–Cz and C4–Cz, respectively (according to the international 10/20 EEG system). C3 and C4 are considered close to the motor area of the arm/hand. C1 and C2 are located closer to the midline and to the motor regions of the legs. In most cases, we obtain responses in both upper and lower limbs with the C1/C2 setup. More details on MEP can be read in Chap. 9. Stimulus parameters include trains of 5–7 stimulus, with a pulse duration of 0.5–0.75 μs and an interstimulus interval of 3–4 ms. The intensity usually does not exceed 200 mA. Lower limb MEPs may be recorded in neurologically intact children with stimulus intensities as low as 60–70 mA. The C1/C2 and C3/C4 setup evoke MEPs from right-side muscles, while the C2/C1 and C4/C3 evoke responses

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from left-side muscles. To selectively evoke lower limb MEPs, Cz′ (placed 1 cm behind the typical Cz setup) to Cz + 6 cm is sometimes preferred, since this setup has the advantage of inducing less neck muscle contraction [25, 26, 34]. The needle electrodes for MEP recording are inserted bilaterally into the muscles, as shown in Table 25.1. To monitor the integrity of the pudendal nerve and for pyramidal motor fibers (for volitional control of the anal sphincter), the needle electrodes are inserted bilaterally into the external anal sphincter. Upper limb MEPs are used only as a control to check on anesthetic interference and rule out problems not related to surgery. It is important to mention that the location of the motor cortex in relation to the coronal suture changes during development. Rivet [35] showed that the distance from the coronal suture to the primary motor cortex increased 1.5 mm per year between the ages of 2 months and 8.6 years. Moreover, the distance from the coronal suture to the motor cortex was 1 segmental level (ipsilateral) 4 – sustained response involving multiple segmental levels and spread to the contralateral leg

Clonic Irregular Sustained Our protocol

a

Table 26.4  Similar classification of EMG response and myotatic reflex SDR reflex grading 0

1 2

3

4

EMG response Unsustained discharge or a single discharge to train of stimuli (ipsilateral) Sustained response only at stimulated segmental level (ipsilateral) Sustained response at level of stimulation and spread within one adjacent segmental level (ipsilateral) Sustained response at level of stimulation with spread ipsilaterally >1 segmental level (ipsilateral) Sustained response involving multiple segmental levels and spread to the contralateral leg

Myotatic reflex grading (/+4) 0/+4

Response No contraction

+/+4

Weak, slight response

++/+4

Brisk reflex

+++/+4

Increased, greater than brisk response, with the absence of clonus Elicitation of clonus and same times contralateral brisk response

++++/+4

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Fig. 26.4  Graphic stimulation threshold (ventral 0,1  mA and dorsal 2,2  mA), tetanic (Phillips classification grade 3 – “sustained” as per Peacock) and free EMG

Although Peacock described several patterns of recognizable neurophysiological abnormalities in the muscles when the dorsal rootlets are stimulated, some of them have no further practical validity [21]. Some patterns, however, could help secondarily in the classification of “normal” or “abnormal” and are worth mentioning. Decremental responses in amplitude, particularly when located in the myotomes corresponding to the stimulation, are considered normal. On the other hand, incremental responses in amplitude and/or sustained responses are considered abnormal mainly if dispersed from the stimulated myotomes [30]. When the Phillips classification is also used, the criteria become clearer (Fig. 26.4). As seen in the descriptions above, this idea has existed since the end of the nineteenth century. It has been progressively improved during the twentieth century to surgically reduce spasticity. Indeed, the use of this type of ablative functional neurosurgery technique has proven effective in combating to spastic sequelae [7, 14– 19, 21]. From Fasano on, the quantitative methodology gave way to the functional approach, based on EMG for the transection of the sick rootlets, introducing electrophysiological recordings [7, 18, 19, 21]. In the Fasano’s primordial works, the muscles of the upper limbs, neck, and face were also monitored, with a spread of discharges captured by EMG being found in these muscles when certain lumbar rootlets were stimulated. This suggested that the presence of this contralateral spread, as well as spread for the upper portions of the body, would be a valid criterion to define that this rootlet is “acting beyond” the medullary-spinal circuit and maintaining spasticity [18, 36, 37]. When analyzing children without spasticity who underwent laminectomy for other situations using electrical stimulation of the posterior root at 50 Hz, Steinbok found 1 of 11 roots with contralateral spread to the muscles of the lower limbs and even to the upper limbs, neck, and face yet minimal and with a nonincreasing pattern, suggesting normality. In turn, in spastic children, this spread was seen more frequently (76%) [27, 30]. In other words, contralateral spreading is an important

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factor in judging the rootlet to be sectioned. Nevertheless, it is important to bear in mind that children without spasticity could present spreading, although less frequently. The neurophysiological criteria for sectioning the rootlets include as an unequivocal “go/cut” responses to tetanic stimulation with Phillips grades 3 and 4. Yet, grades 0–2 mean “spare.” Between 50% and 75% of the rootlets shall be sectioned, ranging from 20% to 80% depending on the clinical behavior for that root [29] (Figs. 26.4 and 26.5). The responses to stimulation are not absolute, clearly, as there is subjectivity to a greater or lesser degree depending on the patient and the “feeling” of the surgeon and team. Depending on the frequency of stimuli, root refractoriness, or suppression of spinal reflexes to the anesthetic agents used, intraoperative conditions can alter motor responses. Electrophysiological responses, however, are reliable enough to represent a safe indication regarding spasticity and strength preservation. Clinical judgment must still prevail, and special care must be taken when deciding the degree

Fig. 26.5  Graphic. Stimulation L2 Right: Threshold (Ventral 0,2  mA and Dorsal 2,4  mA), L2 (adductor)  >  L3 (quadriceps), conduction volume in Hamstring, artefact (out of muscle) Anal Sphincter and Tetanic (Phillips Classification grade 2 – “Incremental” as per Peacock). To section or not would depend on the clinical map and on the “incremental” waveform. In this case it was sectioned

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of injury at S2 for bladder function and whether larger or smaller sections at L4 for knee stability should be made (see below). Consequently, it is extremely important to know in advance the clinical presentation and act on a given root under the anatomical (neurosurgical) and neurophysiological perspective but always correlating with individual patient’s status.

Recording of Threshold and Tetanic Stimulations Each institution has its own method of recording single pulse (threshold) and pulse train (tetanic) stimulations. Ours is shown in Table 26.5.

Root Excitability In relation to the excitability of the dorsal roots, the L2–L3 roots have a modest excitability, and the L4–L5–S1 roots have a high excitability. The manipulation of the roots, either by stretching them when suspending them, or when dissecting them, impacts in a lower responsiveness. It can be a confounding factor when judging the degree of contribution to spasticity considering the Phillips criteria (Tables 26.3 and 26.4) [34]. Table 26.5  Recording of threshold and tetanic stimulations Right Threshold Tetanic grade Threshold Tetanic grade Threshold Tetanic grade Threshold Tetanic grade Threshold Tetanic grade Threshold Tetanic grade Threshold Tetanic grade

Ventral Ventral Ventral Ventral Ventral Ventral Ventral

Dorsal %Cut Dorsal %Cut Dorsal %Cut Dorsal %Cut Dorsal %Cut Dorsal %Cut Dorsal %Cut

L1 L2 L3 L4 L5 S1 S2

Left Threshold Tetanic grade Threshold Tetanic grade Threshold Tetanic grade Threshold Tetanic grade Threshold Tetanic grade Threshold Tetanic grade Threshold Tetanic grade

Ventral Ventral Ventral Ventral Ventral Ventral Ventral

Dorsal %Cut Dorsal %Cut Dorsal %Cut Dorsal %Cut Dorsal %Cut Dorsal %Cut Dorsal %Cut

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L4 and L5 Roots Sectioning Since Foester, the section of L4 and L5 roots has been discussed due to the antigravity function of L4 and the pelvic stability of L5, and, in our view, it should be closely linked to the analysis of the patient’s clinical condition in relation to spasticity and weakness in this region. The assessment should be conducted by a multidisciplinary team, including physiotherapists. The benefit in the specific eligible cases is for ambulation improvement, which should guide the degree of sectioning of the roots [15, 16, 34] (see Tables 26.3 and 26.4).

EMG Artifacts/Pitfalls Artifacts are frequently found and need to be differentiated from activity in response to electrical stimulus. Stimulus artifact is found during simple pulse stimuli (threshold stimulation) and train stimulus (tetanic stimulation). For tetanic stimulation, the artifact appears as a series of individual, thin, equally spaced responses of equal amplitude. The amplitude is proportional to the intensity of the stimulus. This type of artifact is usually greater in channels close to the stimulation site, and usually the impedance is greater in those recording channels. The movement artifact shows a low-frequency oscillation in the recording channels occurring during the movement of the legs or of the electrodes themselves. They may also occur due to electrode displacement (Fig. 26.5). The muscle groups that are most affected by spasticity on clinical examination may present motor unit potentials with a continuous firing pattern around 10–20 Hz (interferential pattern), which hinders the identification of responses to stimulation. This activity can be observed more frequently after stimulation of the roots or rootlets during intraoperative individualization.

Flowchart: Our Routine To carry out neurophysiology in SDR, we must keep in mind what resources we have at our disposal. The minimum to be performed is free-run EMG (fEMG), triggered EMG (tEMG) with threshold, and tetanic stimulation. However, the use of several established intraoperative neurophysiological techniques brings greater safety to the procedure, as recommended for a long time by Dr. Ricardo Ferreira (personal communication) and his team. Flowchart 26.1 shows their assembly. The stability of the transcranial motor evoked potentials (MEP) that are being recorded in the same muscles evaluated by EMG enhances safety. Additionally, the bulbocavernosus reflex (BCR) in conjunction with MEP of the anal sphincter improves the assessment of the sensory and motor pathways of this reflex arc. The

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PATIENT IN THE OPERATING ROOM ANESTHESIA

ELECTRODES PLACEMENT

PATIENT POSITIONING

IONM BASELINES FREE EMG

MEP

PESS

BCR

EEG

BEGINNING INCISION UNTIL DURAMATER OPENING IONM FREE EMG

MEP

PESS

BCR

EEG

LOCATION, SEPARATION AND ISOLATION OF EACH ROOT TO BE EVALUATED FREE EMG

THRESHOLD STIMULATION (ONE PULSE) VENTRAL/ DORSAL? LEVEL?

DORSAL ROOTS OPENED IN ROOTLETS FREE EMG

TETANIC STIMULATION 50 Hz 1 SECOND GRADE 0-2: DON’T CUT* GRADE 3-4: CUT* * ACCORDING TO PATIENT CLINICAL SIGNS

FINAL SDR IONM FINAL FREE EMG

MEP

PESS

BCR

EEG

Flowchart 26.1  Intraoperative neurophysiological monitoring and SDR

electroencephalogram (EEG) helps to check on the anesthetic level, and the somatosensory evoked potential (SSEP) can assess part of the sensitive pathway and even help to compare the ventral or dorsal root. Usually, SSEP is limited in this type of surgery because it is restricted to tibial nerves, identifying compromise focused on the ascending pathways of S1. Note: The abovementioned multimodal techniques are routinely used in IOM and were detailed in the corresponding chapters in this book.

Conclusion SDR is an important part of the therapeutic arsenal available for the treatment of spasticity, especially for children with cerebral palsy. It aims to improve locomotion in cases of ambulatory patients, or to ease the performing of hygiene and comfort care, reducing or removing addictive positions, enabling passive stretching and comfort, and stopping the evolution of deformities. To more objectively perform SDR, the use of neurophysiology through free-run and triggered electromyography

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brings important benefits to the patient. The use of neurophysiological multimodality including MEP, SSEP, BCR, and EEG improves the accuracy of functional assessment. Teamwork enhances patient safety and outcome.

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électrique peropératoire des racines postérieures, et leur utilisation dans le choix des racines à sectionner. Neurochirurgie. 1976;22(1):23–4. 19. Park TS, Gaffney PE, Kaufman BA, Molleston MC. Selective lumbosacral dorsal rhizotomy immediately caudal to the conus medullaris for cerebral palsy spasticity. Neurosurgery. 1993;33:92933. 20. Funk JF, Haberl H. Monosegmental laminoplasty for selective dorsal rhizotomy—operative technique and influence on the development of scoliosis in ambulatory children with cerebral palsy. Childs Nerv Syst. 2016;32(5):81925. Available from: https://doi.org/10.1007/ s00381-­016-­3016-­3. Epub 2016 Jan 13. 21. Park TS, Johnston JM. Surgical techniques of selective dorsal rhizotomy for spastic cerebral palsy. Technical note. Neurosurg Focus. 2006;21(2):e7. 22. Meythaler JM. Concept of spastic hypertonia. Phys Med Rehabil Clin N Am. 2001;12(4):725–32. 23. Abbott R.  Complications with selective posterior rhizotomy. Pediatr Neurosurg. 1992;18(1):43–7. 24. Farmer JP, Sabbagh AJ. Selective dorsal rhizotomies in the treatment of spasticity related to cerebral palsy. Childs Nerv Syst. 2007;23(9):991–1002. 25. Peacock WJ, Arens LJ, Berman B.  Cerebral palsy spasticity. Selective posterior rhizotomy. Pediatr Neurosci. 1987;13(2):61–6. 26. Drazin D, Auguste K. Contemporary dorsal rhizotomy surgery for the treatment of spasticity in childhood. In: Quinones-Hinojosa A, editor. Schmidek & sweet operative neurosurgical techniques: indications, methods and results. Philadelphia: Elsevier/Saunders; 2012. p. 753–8. Selective. 27. Steinbok P, Hicdonmez T, Sawatzky B, Beauchamp R, Wickenheiser D. Spinal deformities after selective dorsal rhizotomy for spastic cerebral palsy. J Neurosurg Pediatr. 2005;102:363–3730. 28. Langerak NG, Vaughan CL, Hoffman EB, et al. Incidence of spinal abnormalities in patients with spastic diplegia 17 to 26 years after selective dorsal rhizotomy. Childs Nerv Syst. 2009;25:1593–603. https://doi.org/10.1007/s00381-­009-­0993-­5. 29. Turner RP.  Neurophysiologic intraoperative monitoring during selective dorsal rhizotomy. J Clin Neurophysiol. 2009;26(2):82–4. https://doi.org/10.1097/WNP.0b013e31819f9077. PMID: 19279497. 30. Hays MH, McLaughlin JF, Bjornson KF, Stephen K, Roberts TS, Price R. Electrophysiological monitoring during selective dorsal rhizotomy, and spasticity and GMFM performance. Dev Med Child Neurol. 1998;40:233–8. 31. Vaughan CL, Berman B, Peacock WJ.  Cerebral palsy and rhizotomy. A 3-year follow-up evaluation with gait analysis. J Neurosurg. 1991;74(2):178–84. https://doi.org/10.3171/ jns.1991.74.2.0178. PMID: 1988585. 32. Clinical practice guidelines for intraoperative neurophysiological monitoring: 2020 update. Special Article. Ann Clin Neurophysiol. 2021;23(1):35–45. https://doi.org/10.14253/ acn.2021.23.1.35. Published online: April 29, 2021. 33. Song Y, Ferri SA, Kobylarz EJ, Thomas Jr GP, Bauer DF.  Advances in neurophysiological intraoperative monitoring during selective dorsal rhizotomy. http://www.asnm.org/resource/ resmgr/Events/2018/Annual/2018_Eposters/5._Song_-­_Advances_in_Neurop.pdf. 34. Phillips LH, Park TS. Electrophysiologic studies of selective posterior rhizotomy patients. In: Park TS, Phillips LH, Peacock WJ, editors. Management of spasticity in cerebral palsy and spinal cord injury. Philadelphia: Hanley and Belfus Inc; 1989. p. 459–69. Neurosurgery: State of the Art Reviews; Vol. 4, No. 2. 35. Dolbow J, Throckmorton Z. Neuroanatomy, spinal cord myotatic reflex. [Updated 2020 Sept 19]. In: StatPearls [Internet]. Treasure Island: StatPearls Publishing; 2021. Available from: https://www.ncbi.nlm.nih.gov/books/NBK551629/. 36. Fasano VA, Broggi G, Zeme S. Intraoperative electrical stimulation for functional posterior rhizotomy. Scand J Rehabil Med Suppl. 1988;17:149–54. PMID: 3165207. 37. Steinbok P, Langill L, Cochrane DD, Keyes R. Observations on electrical stimulation of lumbosacral nerve roots in children with and without lower limb spasticity. Childs Nerv Syst. 1992;8(7):376–82. https://doi.org/10.1007/BF00304784. PMID: 1458494.

Chapter 27

Intramedullary Spinal Cord Tumors Andreya Fonseca Cardoso Cavalcanti, Karina Maria Alécio de Oliveira, Monica Nascimento de Melo, and Silvia Mazzali Verst

Abbreviations CST Corticospinal tract DC Dorsal column DREZ Dorsal root entry zone D-wave Direct wave EMG Electromyography IMSCT Intramedullary spinal cord tumor IOM Intraoperative monitoring ITI Inter-train interval L Lumbar MEP Motor evoked potential Supplementary Information  The online version contains supplementary material available at [https://doi.org/10.1007/978-­3-­030-­95730-­8_27]. A. F. C. Cavalcanti (*) Department of Neurology and Neurophysiology, Neurocol Neurofisiologia Avançada, São Paulo, SP, Brazil e-mail: [email protected] K. M. A. de Oliveira Department of Neurology and Neurophysiology, Clinica Stela de Monitoramento Clínico e Cirúrgico em Neurologia, Brasília, DF, Brazil M. N. de Melo Department of Neurophysiology, Integrated Neuroscience Institute, Goiânia, GO, Brazil S. M. Verst Instituto de Ensino e Pesquisa (Research and Educational Institute) of Sírio Libanês Hospital, São Paulo, Brazil Brain Spine Neurofisiologia, Jundiaí, SP, Brazil © The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 S. M. Verst et al. (eds.), Intraoperative Monitoring, https://doi.org/10.1007/978-3-030-95730-8_27

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mMEP Muscle motor evoked potential NAP Nerve action potential PT Posterior tibial (nerve) SC Spinal cord SCT Spinal cord tumors SEP Somatosensory evoked potential TES Transcranial electrical stimulation Th Thoracic

Introduction Spinal cord tumors (SCT) can be classified based on the location of the tumor as intradural intramedullary, intradural extramedullary, or extradural. The majority of spinal tumors are extradural, accounting for 60% of SCT, and are frequently metastatic lesions. The most common intradural extramedullary lesions are meningioma and schwannoma [1]. Extramedullary intraspinal tumors (intra- or extradural) represent another category of spinal tumors. Some neurophysiological techniques of intraoperative monitoring (IOM) of these pathologies (such as nerve root mapping and bulbocavernosus reflex) have already been covered in Chap. 26. In this chapter, we will address intradural intramedullary tumors and the particularities of their IOM. Intramedullary spinal cord tumors (IMSCT) are rare pathologies. They correspond to 2–4% of central nervous system tumors [2] and 10% of spinal tumors [3], with ependymomas (60–70%), astrocytomas (30–40%), and hemangioblastomas (3–8%) being the most frequent histological types [2, 4–7]. SCT often present first with progressive local or radicular pain, and then other symptoms appear, including weakness, generalized numbness, paresthesias, loss of proprioception, gait imbalance, and sphincter dysfunction [8]. Surgical resection continues to be the most effective treatment modality for most intramedullary tumors, with gross total resection aiming to preserve neurological function and improve survival [9]. However, surgical treatment is often difficult and carries significant risk of postoperative neurological complications. IOM has been shown to be of clinical importance in the surgical resection of IMSCT [10]. The neurophysiological strategy in IMSCT resection surgeries must take into account five fundamental points: (1) the anatomical landmarks of the spinal cord (Fig. 27.1); (2) the safe entry zones; (3) the surgical strategy; (4) the oncological strategy; and (5) the expectation of the functional outcome [11]. There are different aspects related to the pathology of IMSCT that will determine different surgical and neurophysiological strategies. The approach is largely dependent on tumor histology and patient functionality [11]. Tumors that are well demarcated (e.g., ependymomas, hemangioblastomas) can be resected for cure, while more infiltrative tumors (e.g., high-grade astrocytomas)

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Ventral CST Gracile fasciculus Rubrospinal tract

Cuneate fasciculus Lateral CST

Cervical

Long propriospinal tract Posterior spinal arteries

Thoracic

Anterior spinal artery

Lumbar Short propriospinal tract

Fig. 27.1  Cervical, thoracic, and lumbar spinal cord segmentation. Lateral CST carries 85% of all fibers, mainly fast synchronized fibers, and is analyzed by D-wave. Ventral CST carries about 10–15% of total fibers. Both end at the second motor neuron at the anterior horn, mostly through interneurons connections. Short propriospinal tract connects up to six spinal segments, while long propriospinal tract connects cervical to lumbar segments. Anterior spinal artery irrigates anterior two thirds of the spinal cord. Thus, its ischemia or spasm is translated by motor deficit. There are two posterior spinal arteries responsible for irrigation of the posterior third spine. At the posterior funiculus, gracilis and cuneiform tracts transit, medially and laterally, respectively. (@ copyright from Silvia Mazzali-Verst (editor))

are typically managed with biopsies or limited resections in order to minimize the significant risk of damage to the spinal cord (SC) [12]. The use of IOM and the choice of appropriate neurophysiological techniques may help guide the extent of surgery while minimizing damage to normal tissue [10, 11].

IOM Modalities Applicable in IMSCT Resection Surgeries IOM of the functional integrity of SC pathways is crucial to prevent and limit surgically induced injury [10, 13–16]. The available methods can be divided into monitoring and mapping techniques.

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Motor evoked potentials (MEPs), including the D-wave recording, and somatosensory evoked potentials (SEPs) with established interpretation and warning criteria are used for the purpose of monitoring [17, 18]. However, monitoring only provides information about integrity, not about the location and somatotopy of long tracts. Mapping methods are able to identify SC structures [15, 19]. Three methods have been described to map the dorsal column (DC): (1) peripheral nerve stimulation and SEPs recording over the DC using a miniature multi-­ contact electrode [15, 20, 21]; (2) DC stimulation and phase reversal SEPs recording over the scalp [22]; and (3) DC stimulation and antidromic responses recording over peripheral nerves [23]. Three methods have also been reported to map the corticospinal tract (CST) in the SC: (1) the D-wave collision technique [20, 24]; (2) the evocation of muscle responses in the limbs after direct SC stimulation [24–28]; and (3) a more refined and selective stimulation through the double-train stimulation technique [29, 30].

Methodology SEPs Monitoring The stimulation and recording methodology for obtaining SEPs has already been well detailed (see Chap. 8). Posterior tibial (PT) SEPs monitoring is important during an IMSCT resection, due to the high risk of the gracilis tracts damage during myelotomy and tumor dissection. In cases of cervical tumors, the upper limb SEPs should be added. Most patients with IMSCT already have an impaired large fiber sensory system, resulting in lower limb basal SEPs with small amplitudes, increased latencies, and poor morphology. Therefore, an effort should be made to obtain reliable baselines.

Muscle MEPs Monitoring The stimulation and recording methodology for obtaining muscle MEPs (mMEPs) has also been well detailed in another chapter, including the transcranial electrical stimulation (TES) facilitation techniques to try to optimize the baselines, often difficult to record in symptomatic patients (see Chap. 9). The extent of the myotomes sampling should be individualized to the level of surgery (see Chap. 3) and also to the patient’s preoperative neurological status. The greater the number of muscle channels used, the greater the possibility of obtaining reproducible and reliable baselines. The tumor growth can cause dispersion of the fibers of the CST, and the limited number of monitored muscles can lead to false negative results (see Chap. 9).

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Therefore, for high cervical injuries, it is recommended to record all cervical innervation myotomes and at least two or three more muscles of each lower limb (see the suggested myotomes sampling for cervical spine surgeries in Chap. 25). For lesions below Th1, it is recommended to record all lumbosacral myotomes, including the anal sphincter (see the suggested myotomes sampling for thoracic spine surgeries in Chap. 23).

D-Wave Monitoring Direct (D) corticospinal tract (CST) discharges are descending volleys registered on the first motor neuron axon within SC. Mostly, D-wave is the potential of CST fast-­ conducting fibers of lateral funiculus. Several D-waves are generated after short train stimulation of motor cortex, and they will be responsible for second motor neuron activation and consequent mMEP. Conversely, in order to intraoperatively evaluate D- wave, single anodic pulse is used through TES [31]. An extensive and detailed explanation about D-wave anatomical bases and its methodology was covered in the chapter about motor evoked potential (see Chap. 9). Here we will review the key points about stimulation and recording and practical tips to improve D-wave acquisition. Anatomical and functional basis of SC sources for D-wave and mMEP are different. CST originates from premotor frontal lobe, postcentral, and precentral gyrus. The latter counts for approximately 80% of its origin. Around 85% of CST fibers decussates at the pyramids and runs at SC lateral funiculus. They are the ticker myelinated synchronized fibers of the motor tract and are mostly related to fine coordinated movements [10, 15, 32]. A small percentage connects directly to the second motor neuron, while the remaining fibers terminate on propriospinal interneurons. In fact, most input to alpha motor neurons originates in interneurons, building a complex network of connections. This neural network links somatosensory and proprioceptive information with motor control. Long and short propriospinal tracts integrate multiple spinal segments [32, 33] (Fig. 27.1). D-wave corresponds to direct recording of the descending volley at the lateral funiculus, while mMEP is a product of alpha motor neuron activation and motor units’ depolarization (see Chap. 9). Combining the use of D-wave and mMEPs provides the most comprehensive assessment of the SC motor tracts’ functional integrity during surgery for IMSCT [15]. It is considered the gold standard. For D-wave recording, the catheter electrode (Fig. 27.2) may be sited both rostrally (as a reference) and caudally (as active electrode) to the tumor, at the epidural or subdural space. Once placed, the best combination between two of the electrode tips 1, 2, and 3 is tested to ensure the highest possible D-wave amplitude. D-wave is usually recorded in 20 ms epochs and amplified 10.000 times with filter settings of 1.5 ± 1700 Hz [31]. Low impedance values improve quality of recordings. The most efficient pulse duration is 0.5 ms because it allows for the quicker recovery of each

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Fig. 27.2  D-wave catheter

Table 27.1  Summary of the stimulation and recording methodology for obtaining the D-wave Stimulation Scalp Montage: C1/C2, 6 cm/Cz or C3/C4 Electrodes Corkscrew electrodes Parameters Anodic single pulse Duration: 0.5–1.0 ms Frequency: 0.5–2.0 Hz

Site

Recording Epidural or subdural space (below the lesion) D-wave catheter Screen: 30 μV/div and 1–6 ms/div Sweeps: 20 ms Filter settings: 1.5 ± 1700 Hz

consecutive D-wave amplitude [15]. The choice for scalp electrodes montage remains of some debate. Either montage C1–C2 or C3–C4 will work fine. Choose the one that results in less neck movement, so that it allows for continuous D-wave monitoring at a rate of 0.5–2 Hz. The stimulation and recording methodology of the D-wave monitoring technique [31, 34] is summarized in Table 27.1. D-wave amplitude reaches approximately 80 μV at cervical region (Fig. 27.3) and half this amplitude by lumbar spinal cord (at the vertebral level of Th10) [15]. Below Th10 there is a small amount of recordable CST running to conus medullaris at L1. D-wave is quite unrecordable [35]. Amplitude variation from trial to trial of 10% is acceptable. Expected latencies increase when the recording site is moved caudally. Reference values are 3–6  ms at cervical region and 6–9  ms at thoracic region [34, 35]. D-waves can be evaluated during intra-axial supratentorial, cervical-bulbar, and SC approaches. During mid-low cervical IMSCT resections, the electrode is located below vertebra C7, and it will record thoracic and lower limbs CST only. For upper cervical SC level surgery, electrode may be placed at lower cervical levels. In conclusion, D-wave translates the CST running along the surgical field but not of the segmental spinal cord. Hence, selection of segmental muscles to record from is an important issue in the monitoring of mMEPs in order to ensure selectivity. Additionally, selection of the atrophied muscles is nonoptimal and hinders monitorability. Taking care to needling the muscle motor point is standard of care (more details in Chap. 3).

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a

593

b

c

Fig. 27.3  Muscle MEPs and D-waves recordings in a 65-year-old woman who underwent resection of a C1–C5 ependymoma. (a) Preoperative MRI. (b) Basal mMEPs (lower image) and D-waves (upper image). (c) Continuous D-wave monitoring. Total tumor resection without intraoperative neurophysiological changes (stable mMEPs and D-waves). Postoperative outcome without new neurological deficit. The traces in red color correspond to baselines. E, left; TRAP, trapezius; DELT, deltoid; BR, brachioradialis; ECD, extensor digitorum; APB, abductor pollicis brevis; TA, tibialis anterior; AH, abductor hallux; XII, genioglossus

Motor outcome prognosis during IMSCT resection can be predicted by IOM changes. Fundamentally, a combination of D-wave and mMEP is analyzed (Table  27.2). Physiological basis for understanding this behavior lies on SC functional architecture. mMEP is dependent on the positive and negative inputs to the alpha motor neuron, through interneurons and originating from different tracts. Intramedullary manipulation during tumor resection may result in disorganization of this system and mMEP deterioration or loss. Yet, postoperative neuroplasticity is mostly related to propriospinal tracts, due to their greatly innate regenerative capacity [33]. Conversely, D-wave deterioration means axonal loss and there is less room for recovery. Thus, the long-term postoperative

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Table 27.2  Using the mMEP and D-wave data to guide surgery and predict outcome mMEPs No change ↓ Amplitude ↑ Threshold

D-wave amplitude No change No change or >80% of baseline

Lost

No change or >80% of baseline

Lost

Reaching 80% of baseline

Lost

Below 50% of baseline

Surgeon response None Tip:  Time/break  Irrigation  Pressure improvement  Use of papaverine Tip:  Time/break  Irrigation  Pressure improvement  Use of papaverine  Proceed with caution  Consider Stop Stop

Postoperative motor function Same as preoperative Same as preoperative or transient deficit

New deficit that often improves

High risk for permanent deficit

Permanent new deficit; possible plegia

Source: Reproduced from Sala et al. [36] (with permission)

motor prognosis is highly dependent on the stability of the D-wave amplitude (Fig.  27.4) during the intraoperative period (preservation of at least 50% of D-wave amplitude) [10, 15, 32, 37]. D-wave is recordable in two thirds of the patients [38]. Failure is believed to be related to desynchronization of the wave if motor status is preserved.

Free Electromyography Monitoring After the description by Skinner et al. in 2009 on the correlation of suprasegmental electromyography (EMG) discharges and mechanical irritation of CST fibers [39], several other authors began to value free-run EMG recordings during surgeries for resection of brain and SC tumors [40]. In this context, the presence of EMG discharges may alert to the need to intensify surveillance in the MEP (see Chap. 11).

Dorsal Column Mapping Techniques Retrograde Recording of Posterior Tibial Nerve Action Potentials (NAPs) The recording of the posterior tibial (PT) NAP after DC stimulation with bipolar handheld electrode is a time-consuming and poorly reproducible antidromic technique for mapping the DC.

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a

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b

c

d

Fig. 27.4  Muscle MEPs and D-waves recordings in a 25-year-old man undergoing resection of a cervicothoracic astrocytoma. (a) Preoperative MRI. (b) Continuous and stable D-wave monitoring. (c) Preserved D-wave amplitude (lower image) and an important drop in the amplitudes of the lower right limb mMEPs (upper image). The slight delay in D-wave latency may be related to a small displacement of the catheter. (d) Complete disappearance of lower limb mMEPs (upper image), maintaining amplitude stability of D-wave (lower image). Total tumor resection without D-wave changes. Immediate postoperative status was paraplegia. After 3 months of motor rehabilitation, patient showed complete neurological recovery. IOM mMEPs disappearance led to a transient paraplegia. The traces in red color correspond to baselines. E, left; TRAP, trapezius; DELT, deltoid; BR, brachioradialis; ECD, extensor digitorum; APB, abductor pollicis brevis; TA, tibialis anterior; AH, abductor hallux

The method was described by Quinones-Hinojosa et al. in 2002, who suggested its use in identifying the median raphe for performing midline myelotomy in IMSCT resection surgeries [23]. The stimulator probe should be positioned with the cathode tip pointing distally to the longitudinal axis of the spinal cord, starting 2 mm lateral to the presumed midline. As the PT NAPs appear after at least about 50 averages, the probe should be moved 1 mm lateral to the presumed midline, and a new attempt at stimulation should be performed, comparing the amplitudes of the NAPs according to the displacement of the stimulator. This procedure is repeated on the contralateral side of the presumed midline. The region of complete absence of response or lowest amplitude is assumed to be the region with the fewest number of axons (functional midline). When it is not possible to visualize any anatomical outline of the midline (in cases of distortion of the fibers of the DC by the tumor), a good alternative is to perform the stimulation by moving the probe several times every 1 mm from the

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extreme left to the extreme right (or vice versa) in the dorsal aspect of the SC. The disappearance of the NAP will indicate the location of the median raphe. The stimulation and recording methodology of this retrograde recording of PT NAPs technique [23] is summarized in Table 27.3. Antegrade Recording of Spinal SEPs The principle of this method is based on the fact that at the level of the gracilis tracts, the recorded electrical volleys triggered by peripheral stimulation of the ipsilateral posterior tibial nerve will have the highest amplitudes, thus enabling the identification of the neurophysiologic midline (median raphe) [18, 41]. Table 27.3  Summary of the stimulation and recording methodology of the three dorsal column mapping techniques Retrograde recording of Technique PT NAP Stimulation Recording Site Spinal cord Posterior tibial nerves: (DC) Parallel to  Ankle (medial the spine malleolus) axis  Popliteal Cathode fossa pointing distally A pair of Electrode Bipolar electrodes: handheld Subdermal electrode needle 2–3 mm between the tips Sensitivity: Parameters Pulse 1–5 μV duration: Time base: 0.2 ms Intensity: 100 ms Bandpass: 3–8 mA Frequency: 30–300 Hz 9.1 Hz 50–100 trials

Antegrade recording of spinal SEPs Stimulation Recording Spinal cord Posterior tibial nerves: (DC) Perpendicular  Ankle to the spine (medial malleolus) axis Equidistant referential recording A pair of 8-contact electrodes microelectrode Referential recording:  Subdermal needle Identical to Sensitivity: those used for 10–50 μV Time base: the SEPs monitoring 50 ms Bandpass: technique (see Chap. 8) 50–1700 Hz  Pulse duration: 0.2 ms  Intensity: 40 mA  Frequency: 13.3 Hz  100–200 averages

Phase reversal technique Stimulation Recording Spinal cord Scalp recording: (DC) Parallel to   CP3–CP4 the spine  CPz–Fz axis Cathode pointing proximal Corkscrew Bipolar electrodes handheld electrode 2–3 mm between the tips Sensitivity: Pulse 1–5 μV duration: 0.2–0.3 ms Time base: 50 ms Intensity: 0.2–0.5 mA Bandpass: Maximum 30–300 Hz intensity: 1 mA Frequency: 3.17 Hz 10–20 trials

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This DC mapping method has been described for use with an electrode specifically developed for this purpose: a miniature multielectrode grid, consisting of eight parallel stainless-steel wires (numbered 1–8), with 76  μm diameter and spaced 1 mm apart [15, 20]. Other authors have reported intraoperative SEP recordings in the DC using other types of electrodes. However, these recordings (with silver ball and stainless-steel disc electrodes) were used for monitoring in order to avoid DC injuries in ablative procedures, but not for mapping purposes [42–46]. The multielectrode GRID was developed to reliably record high-quality TP spinal SEPs over the cervical and thoracic SC. The electrode size was appropriate to the size of the DCs according to anatomical studies [30]. The neurophysiological or functional midline was determined to lie between the two recording sites with highest SEP amplitudes after stimulation of either left or right tibial nerve. In patients with cervical lesions, it is recommended also to record spinal SEPs after median nerve stimulation. The recorded potentials consisted mainly of segmental responses (stationary waves). An amplitude gradient across eight recording sites was also observed, with highest amplitudes of SEPs laterally, close to the dorsal root entry zone (DREZ). Lower amplitudes were observed toward the dorsal midline contrary to recorded SEPs following PT nerve stimulation. Median nerve stimulated segmental potentials have the maximum amplitude lateral due to the lateral position of the dorsal horn (gray matter); PT nerve SC conducted SEPs have the highest amplitude medial as they are conducted via the fasciculus gracilis [21, 30]. The spinal SEPs recorded after median nerve stimulation were only helpful in determining the functional midline indirectly, indicating proximity to the DREZ.  Therefore, median nerve stimulation can be useful in mapping of the DREZ.  Nevertheless, the midline in the cervical SC could successfully be determined using PT nerve SEPs [21, 30]. The stimulation and recording methodology of the antegrade recording of spinal SEPs technique [30, 41] is summarized in Table 27.3. In the same way as the DC mapping technique via antidromic recording of NAP, this technique of orthodromic recording of spinal SEPs via miniature multicontact electrode has also not become popular among neurosurgeons and neurophysiologists. This FACT can be attributed to some disadvantages of its use: the recording electrode is too rigid and does not adhere well to the spinal cord; the arterial pulsation of the medullary vessels under the electrode generates many artifacts, making poor the signal-to-noise ratio; it has high cost and difficult electrode availability and wide variability in the recording amplitude. In short, it is a method that is difficult to apply and poorly reproducible and that demands a lot of time for surgeons.

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 nterograde Recording of Cortical SEPs: The Gracilis SEP Phase A Reversal Technique SC stimulation with cortical SEP recording has been reported since 1986 [47, 48] but as a monitoring method, not as a mapping technique in an attempt to identify the median raphe. The gracilis SEP phase reversal technique, as a mapping technique, was described by Simon et al. [49]. It is a method that uses phase reversal SEPs recording over the scalp after direct DC stimulation [22]. Initially stimulated via an eight-contact electrode, Simon et al. later used a bipolar handheld stimulator placed parallel to the longitudinal axis of the cord. Stimulating the medial part of the right DC depolarizes the right gracilis tract and thus generates cortical SEPs with the same polarity as if we were stimulating the right PT SEPs. This translates in the CP3–CP4/CP3–Fz channel in a negative upward peak (or in a CP4–CP3/CP4–Fz potential in the reversed positive downward deflection) equivalent to the P37 potential but occurring earlier (Fig.  27.5 and Video 27.1). Moving the bipolar stimulator to the left and crossing the median raphe, stimulation of medial part of the left DC depolarizes the left gracilis tract; thus the polarity in the CP3–CP4 channel reverses, showing a positive, downward peak (Fig. 27.5). The SEP recorded in the CPz–FPz channel should always show a positive peak, regardless of the site (right or left) of stimulation (Video 27.1). Stimulation of the raphe should not result in reproducible SEPs, in neither CP3–CP4 nor CPz–FPz channels. And current spread with simultaneous stimulation of both gracilis tracts will result in cancelation of the potentials in the CP3–CP4 channel, however robust positive potentials in the CPz–FPz channel. Unlike the spinal SEPs, which tend to have a more complex polyphasic morphology, the gracilis SEPs mirror the P37/N45 morphology, at shorter absolute latencies. The more distal the spinal stimulation is applied, the longer the latency of the response will be. The reported absolute latencies on the thoracic level are around

Fig. 27.5  Dorsal column mapping: DC stimulation and phase reversal SEPs recording over the scalp. Stimulation at three different points of the spinal cord: left DC (upper tracing), midline (middle tracing), and right DC (lower tracing). (Source: Renê Werton Veras, MD (neurophysiologist), and Iuri Neville, MD, PhD (neurosurgeon). Unpublished personal data (with permission))

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12–20 ms and on the cervical level are around 8–11 ms. However, surgical level, infiltrating, or compressing tumors of the SC significantly affect latencies. The stimulation and recording methodology of this phase reversal technique is summarized [22, 49] in Table 27.3. When compared with other methods, the signal-to-noise ratio of the recorded responses is significantly higher due to the thalamocortical amplification of the evoked potentials. Thus, it requires fewer averages, making the technique more reproducible and less time-consuming. Among the three techniques described, the authors’ experience is greatest with the gracilis SEP phase reversal technique. However, regardless of the technique chosen, it is important to emphasize two fundamental actions for the correct interpretation of the DC mapping: 1. Comparison with basal PT SEPs 2. Carrying out the mapping at all levels of the spinal cord that will cover the extent of the myelotomy By analyzing the basal PT SEPs, it is possible to recognize any preexisting asymmetries. In this case, there will be probably also asymmetry of the right/left SEPs recorded by one of these three mapping techniques. The side of the fasciculus gracilis that is more compromised or “negatively mapped” can be chosen as the site of myelotomy, rather than the median raphe itself. The important issue is to choose a neurophysiologically silent area, which could be the median raphe or an area supposedly already damaged by the tumor. Mapping all of the spinal levels is important as the trajectory of the median raphe can change significantly from one column level to the next.

Motor Pathways Mapping Techniques D-Wave Collision Technique The D-wave collision technique consists of activating the CST by simultaneous TES and direct SC stimulation [24]. Continuous TES causes a descending volley, which is recorded via spinal electrodes as D-waves. Intermittently, the surgeon also stimulates the exposed spinal cord, via a handheld stimulator probe delivering a single stimulus of 1–2 mA intensity. Since the resulting signals are transmitted along the same CST axons, the descending D-wave collides with the ascending signal carried antidromically along the CST [20]. When the probe is in close proximity to the CST, it depolarizes and causes an antidromic volley, which is expected to collide with and annihilate the D-wave. Thus, the disappearance or the decrease in the D-wave amplitude helps identify the location of the CST. However, it is not an easy reproducible method.

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Direct Stimulation of the SC to Elicit Responses from Limb Muscles Based on experiences of direct motor stimulation in cranial surgeries, many authors have tried to apply the Penfield method (see methodology in Chap. 17) to map the CST during SCT resection surgeries. Many attempts have been described so far for motor mapping in SCT surgery [26, 27], mostly using a bipolar handheld stimulator and observing triggered movements in different muscles and limbs (Fig. 27.6). R

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Later, Gandhi et al., using the same Penfield paradigm, expanded muscle sampling and used a concentric bipolar stimulator. Thus, they were able to provide a more delicate and more selective stimulation of the CST fibers [25]. As with subcortical motor mapping of the CST in supratentorial surgery (see Chaps. 14 and 17), some authors [28, 40] have been successfully using high-­ frequency cathodal monopolar stimulation to map the CST at the cord level. It consists in applying repetitive trains at 1–2  Hz, with 4–6 pulses/train, and a pulse duration of 0.5 ms. It can also be applied continuously, with the cavitronic ultrasonic surgical aspirator (CUSA), allowing simultaneous mapping and resection of the tumor [28]. In this case, it is recommended to use a short train of cathodal pulses (3 pulses, 0.2 ms pulse duration, interstimulus interval 3 ms) with an intensity ranging from 0.5 to 2  mA and recordings from limb muscles [28]. However, stimulation of cord tissue can be non-focal, resulting in confusing interpretation. Despite the limitation of this direct SC stimulation technique, it has its benefits mainly in cases of absence of basal D-wave recordings. Double-Train Stimulation Technique The main problem related to proposed techniques for mapping the CST in the SC is related to the lack of selectivity of the motor response obtained. Responses recorded from limb muscles after stimulation of the exposed SC can also be obtained by stimulation of the DC and not exclusively by stimulation of the CST [29, 30]. Deletis et al. demonstrated that muscle responses after CST or DC stimulation have distinguishable features if double-train stimulation is used [30]. The spinal interneurons targeted by CST fibers have a much shorter recovery time than 60  ms (see Chap. 9). Meanwhile, the spinal interneurons targeted by branches of DC fibers ending up to the alpha motoneurons as a part of reflex arc have a recovery time significantly longer than 60 ms [50]. It is expected that CST stimulation with 60 ms inter-train interval (ITI) would generate a response after the second train, whereas stimulation of the DC would not do so. Therefore, mapping of the exposed SC can be performed with a doubletrain stimulation paradigm [30]. If a response in a limb muscle appears after the first as well as after the second stimulus train, this indicates that the stimulating electrode is in close proximity to the CST. If there is no response to the second train of stimuli, this indicates that the electrode is in close proximity to the DC, because interneurons targeted by DC fibers are still in the refractory period (Fig. 27.7). This concept might improve the intraoperative SC mapping especially in tumors with infiltrative margins such as astrocytoma, where it is difficult to establish a clear resection plane.

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Fig. 27.7  Consecutive trials of double-train stimulation (stim) of SCT and DC with an inter-train interval of 60 ms and muscle recordings. Patient with an intramedullary pilocytic astrocytoma at the C2–Th1 level. Stimulation of the SCT with double trains of stimuli elicited identical double responses in the resection cavity (upper image). Stimulation of the DC elicited only one response after the first train, but no response after the second train (lower image). Identification of both tracts guided surgery with continuous mapping during tumor removal providing real-time neurophysiological feedback of the location of those tracts. AH, abductor hallucis; APB, abductor pollicis brevis; EXT, extensor digitorum; TA, tibialis anterior. Probe indicates the stimulating probe. (Source: Reproduced from Deletis et al. [30] (with permission))

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Critical Surgical Times and Neurophysiological Techniques Table 27.4 systematizes the neurophysiological modalities that should be applied in each of the different surgical steps of SCT resection surgery.

Interpretation SEPs and MEPs monitoring are important during an IMSCT resection, due to the high risk of the gracilis tracts and CST damage during myelotomy and tumor dissection. However, the primary objective of IOM in SCT resection surgeries is to preserve the CST and distal motor function. And the gold standard is through continuous and combined monitoring of mMEPs and D-waves. Muscle MEPs are the result of depolarization of the alpha motor neuron, not only by the CST but also by other descending tracts, such as the propriospinal tract, which could be injured during myelotomy and tumor resection. Their injury causes immediate significant but not selective changes or disappearance of the mMEPs. Additionally, desynchronized electrical volleys on CST primary axons may not contribute to D-wave amplitudes. Thus, their damage may not be detected by changes in D-wave amplitudes. To detect early injury to the CST in SCT surgeries, the recommended alarm criteria are based on the combined information of mMEP and D-wave monitoring, and

Table 27.4  Proposed neurophysiological monitoring protocol for each of the surgical steps for intramedullary tumor resection Anesthesia Positioning, opening and dissection of muscle planes, laminectomy to dura opening Immediately before and during dura opening

Immediately after dura opening Immediately before the myelotomy (to identify median raphe) During myelotomy During tumor resection Advancing in tumor resection End of tumor resection until closing

Placement of electrodes SEPs and mMEPs baselines SEPs and mMEPs New SEPs and mMEPs baselines Add D-wave recording (with epidural catheter placement) SEPs, mMEPs, and D-wave (now with subdural catheter placement) DC mapping (with the technique with which you have more experience) New SEPs, mMEPs, and D-wave baselines SEPs and D-wave SEPs, mMEPs, and D-wave Pause for mapping the SCT (if the surgeon deems to do so) Last record of the D-wave Catheter removal SEPs and mMEPs to skin suture

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mostly on the measurement of the D-wave amplitude [14, 15, 37]. Yet, there is still controversy in relation to a strictly numerical “cut-off” of the D-wave amplitude drop. Controversy includes also disappearance of mMEPs as superior to its amplitude drop or stimulation threshold increase [40]. Alarm criteria for mMEP changes differ depending upon the type of surgery and the mechanism of injury (see Chap. 9) [51]. If there is a significant reduction in mMep amplitude, the neurophysiological recommendation is to immediately stop the surgical manipulation for at least 30 min or until recovery, irrigate the surgical field with warm saline including papaverine, and elevate mean arterial blood pressure [36]. The decision to continue or discontinue the procedure will depend on the recovery level of the mMEPs and the amplitude status of the D-wave [37] (Fig. 27.8). In general, patients who experience a complete loss of mMEP, but D-wave amplitude preserved to at least 50% of baseline, would sustain only a transient new motor deficit [14, 36, 52]. However, some authors reported new and irreversible postoperative motor deficit in this situation [40, 53]. Thus, Mirela et  al.

a

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Fig. 27.8  Female, 52  years old, evolving with asymmetric tetraparesis and gait ataxia due to extensive cervical intradural and intramedullary lipoma (C1–Th1). There was drop in the mMEP and D-wave amplitudes during the surgical manipulation. It was followed by a complete improvement in the D-wave and almost complete improvement in the mMEPs. Subtotal tumor resection and C3 to Th4 arthrodesis were performed. Immediate postoperative: worsening of tetraparesis. After 6  months of follow-up, patient recovered to initial preoperative clinical tetraparesis. (a) Preoperative MRI. (b) Onset of instability and drop in amplitude of mMEPs. (c) 50% drop in the D-wave amplitude. (d) Partial recovery of mMEPs. (e) Full recovery of D-wave. (f) Final mMEPs (partial recovery, no return to baseline status). (g) Pre-tumor resection and post-arthrodesis surgical image. (h) Surgical image after tumor resection. The traces in red color correspond to baselines. E, left; TRAP, trapezius; DELT, deltoid; BR, brachioradialis; ECD, extensor digitorum; APB, abductor pollicis brevis; TA, tibialis anterior; AH, abductor hallux. (Source (g) and (h): Courtesy of neurosurgeons Chrystiano Fonseca Cardoso, MD, and Alessandro Fonseca Cardoso, MD. Unpublished personal data (with permission))

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recommended a more conservative approach: in the case of total loss of mMEPs, the resection can be safely continued only if D-wave remains at least 80% of baseline (very close to baseline). Mirela et  al. agree that a drop in the averaged D-wave recordings of more than 20% from baseline should be considered a warning sign. Table 27.2 summarizes the correlation that should be made between the interpretation of neurophysiological changes and the surgical approach to be taken, as well as the expected postoperative neurological functional outcome.

Conclusion Surgical approach remains the main way of treatment for patients with IMSCT. The goal is achieving maximum safe tumor resection, maintaining functional neurological viability. IOM is responsible for revisiting old paradigms in IMSCT treatment, such as that they are synonymous of inoperable injuries. Choosing appropriate neurophysiological techniques can help to guide the extent of surgery, minimizing damage to normal tissue. IOM techniques have greatly evolved in recent years beyond the continuous monitoring of the long pathways through SEPs, mMEPs, and D-waves. DC mapping has become a reliable technique and the CST mapping is just a step ahead. Currently, the refinement of these alarm criteria has contributed to improve the neurological outcome.

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Part VI

Vascular Surgery

Chapter 28

Intraoperative Neurophysiologic Monitoring of Cerebrovascular Disorders Jaime R. López and Felix W. Chang

Abbreviations ACA Anterior cerebral artery APB Abductor pollicis brevis AVMs Arteriovenous malformations BAEP Brainstem auditory evoked potential CCT Central conduction time CDSA Color density spectral array CI Confidence interval CTA Computed tomography angiogram dcMEP Direct cortical motor evoked potential DSA Density spectral array EC-IC Extracranial-intracranial EEG Electroencephalography EMG Electromyography FDI First dorsal interosseous ICA Internal carotid artery INR Interventional neuroradiology

J. R. López (*) Department of Neurology and Neurological Sciences, Stanford University, Stanford, CA, USA Department of Neurosurgery (Courtesy), Stanford University, Stanford, CA, USA e-mail: [email protected] F. W. Chang Department of Neurology and Neurological Sciences, Stanford University, Stanford, CA, USA © The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 S. M. Verst et al. (eds.), Intraoperative Monitoring, https://doi.org/10.1007/978-3-030-95730-8_28

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IONM Intraoperative neurophysiologic monitoring mA Milliamps MAP Mean arterial pressure MCA Middle cerebral artery MEP Motor evoked potential mRS Modified Rankin score mTICI Modified thrombolysis in cerebral infarction grading NIRS Near-infrared spectroscopy OR Odds ratio OR Operating room qEEG Quantitative EEG rCBF Regional cerebral blood flow rSO2 Regional saturation of oxygen SSEP Somatosensory evoked potentials STA Superior temporal artery TCD Transcranial Doppler TcMEP Transcranial motor evoked potential

Introduction Intraoperative neurophysiologic monitoring (IONM), the use of neurophysiologic testing intraoperatively to monitor the integrity of neural structures, has seen increasingly widespread use in a variety of procedures over the last several decades. The surgical and endovascular treatment of cerebrovascular disorders is an area where IONM has seen great growth, and in some institutions, it now plays the role of an indispensable adjunct for these procedures. IONM is able to identify cerebral ischemia, one of the most feared complications of these types of procedures. It can also indirectly identify hemorrhage, another potential complication. The ability to identify and reverse cerebral ischemia using different techniques is important in increasing the safety of cerebrovascular procedures. There are several electrophysiologic techniques which have been demonstrated to be useful for the purpose of improving neurologic outcomes by identifying and potentially reversing intraoperative cerebral ischemia. The goals of this chapter are to discuss the types of cerebrovascular procedures in which IONM is utilized, the different IONM techniques that can be used in monitoring these procedures, the physiologic rationale for why these techniques can be used, and the expected types of changes in response to cerebral ischemia in these techniques.

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 erebrovascular Procedures Where IONM Is C Commonly Utilized There are a variety of cerebrovascular disorders which are approached both surgically and endovascularly. The most common of these disorders in which IONM is utilized are the following: 1. High-grade carotid artery stenosis 2. Cerebral aneurysms 3. Cerebral arteriovenous malformations (AVMs) 4. Cerebral cavernous malformations 5. Vascular occlusive disorders, e.g., moyamoya disease

 ffect of Regional Cerebral Blood Flow E on Electrophysiologic Studies Cerebrovascular procedures carry the risk of cerebral infarction as they involve the manipulation of the cerebrovascular system, which can cause a number of complications, including thromboses, emboli, vasospasm, vascular occlusion, and hemorrhage. Before discussing specific surgeries, it is important to understand the physiologic basis on which electrophysiologic studies are able to detect ischemia. Electroencephalography (EEG) and somatosensory evoked potentials (SSEPs) have been extensively studied in this context and can indirectly detect cerebral ischemia before it progresses to a cerebral infarct. Their utility for this purpose was established by a series of human and animal studies in the 1970s and 1980s which separately showed a strong correlation between regional cerebral blood flow (rCBF) and changes in EEG and/or SSEP. Several primate studies showed the relationship of rCBF with SSEP amplitude. In Branston et al. [13], they showed that that cortical SSEPs remained present when rCBF was ≥16 ml/100 g/min and became absent at 70% stenosis in the contralateral carotid, and bilateral vertebral stenosis [32, 119, 124]. Interestingly, after controlling for other factors, >70% stenosis in the ipsilateral carotid decreased the odds of EEG changes (OR 0.43), likely reflecting the patient had developed sufficient collateral circulation in chronic carotid stenosis [119]. Anesthesia Anesthetic agents can have a multitude of effects on the EEG, ranging from electrocerebral inactivity, mild slowing, to increasing the frequency. The effects of anesthesia on EEG are typically bilateral and symmetric, which is important in differentiating anesthetic effects from hemispheric ischemia. If the patient has a previous cerebral insult, increased prominence of a previous focal abnormality is possible in response to anesthesia. It is good practice to periodically have the anesthetic levels noted to assess their relation to the EEG. It is common to see increased rhythmic beta (12–18 Hz) activity following induction. This is typically over the anterior hemispheres. As the procedure progresses, and the patient reaches a lighter steady state compared to induction, the amplitude of the EEG typically increases and slows to 8–14 Hz. Intermittent delta activity can be seen anteriorly in this state. At high enough levels of inhaled or intravenous anesthetics, burst suppression and electrocerebral silence can be seen on the EEG. Boluses of narcotics can sometimes induce burst suppression as well (personal observation).

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Technical Factors Ensuring proper electrode placement, intact electrodes, low electrode impedances, and isolation of any ambient electrical noise is important in ensuring a good-quality EEG recording. Knowing how to efficiently troubleshoot to find the technical factors which are interfering with the recording is essential. If these factors are not present, the interpretation of the EEG will be difficult. Critical Intraoperative EEG Changes The most critical point of a CEA occurs at the time of cross-clamping the carotid. If there are ipsilateral EEG changes following cross-clamping, this indicates the presence of cerebral ischemia. To reverse ischemia, cerebral blood flow to the ipsilateral hemisphere must be increased, usually through carotid shunting. Surgeons who are selective shunters and utilize IONM services will typically shunt following major EEG changes. If the EEG changes are mild, raising the MAP prior to shunting may optimize ipsilateral cerebral blood flow to the point where the EEG improves, and shunting is not needed. Of course, the EEG will need to be carefully monitored during the remainder of the shunt period in case evidence of ischemia arise anew. If needed, carotid shunting can be done during any stage of the cross-clamp period. Quantitative EEG Quantitative EEG (qEEG) refers to any mathematical processing of conventional EEG. Conventional EEG may also be referred to as raw EEG, unprocessed EEG, or EEG. There are many different techniques and tools that can be used to analyze the EEG. qEEG in the operating room dates back to the 1970s [20, 87]. As a technique, it has gained increasing popularity as it has become more accessible. In a review of qEEG outside of the OR, Gavvala et al. [44] reported that 52% of neurophysiologists were using qEEG. EEG data is normally viewed in the time domain. The most used qEEG techniques use Fourier analysis to translate the EEG to the frequency domain. The most common way to represent this is the density spectral array (DSA) or color density spectral array (CDSA) [66]. The DSA displays time on the horizontal axis and frequency on the vertical axis and uses color to code the power. Ischemic changes, which include slowing and attenuation of faster frequencies, are visually represented by a change in color (change in power) and downward shift of the main frequency bands. Visually, these are easier to interpret than the same changes would be on the unprocessed/raw EEG (see Fig. 28.1). There have been several studies that have shown the usefulness of qEEG in identifying ischemia and predicting neurologic outcome in CEA, with some authors reporting that they find qEEG more useful than raw EEG [2, 20, 103].

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Fig. 28.1  This figure demonstrates mild hemispheric slowing during a right-sided CEA on DSA. The left and right hemispheres are shown. The y-axis is frequency; the x-axis is time. Low power is shown in cool colors and high power in warm colors. The dotted line is a frequency marker placed to help better visualize changes in frequency. White bars that take up the whole frequency spectrum are times where electrosurgery is occurring and the program has automatically excluded the resulting high amplitude EEG artifact from analysis. A 30-min segment is shown here. A small downward shift in the dominant frequency band of the right hemisphere can be seen in the area highlighted by the red circle. At the same time, a 30% decrease in the amplitude of the left median nerve cortical SSEP also occurred. Both changes resolved when the carotid was unclamped

qEEG is a powerful tool when used correctly but has limitations. It should not be thought of as a replacement for the raw EEG but rather an adjunct. The main advantages of qEEG lie in the ability to see trends develop over longer time scale and scan larger time periods quickly. It is important to confirm any suspected findings on qEEG with the raw EEG. Rhythmic artifacts, common in the OR, can frequently mimic the appearance of physiologic signals on DSA. DSA is well-suited for purposes such as assessing the change in depth of anesthesia over the course of the case. In the context of IONM, it may be easier to observe subtle ischemia on qEEG than raw EEG, as one can more easily detect smaller changes in frequencies. As monitoring of simultaneous cases continues to grow, the advantage in time may also become more important. Looking at the DSA provides less real-time information than the unprocessed EEG. This is because Fourier analysis is performed on discrete time epochs, often around 8  s in length. It likely will take several epochs before a trend becomes apparent on the DSA, which can represent a lag of 30 s or more from when a change might first be apparent on unprocessed EEG. For critical time points, such as cross-clamping, this may not be ideal. In Kearse et al. [61], a prospective study of 103 CEA patients, EEG and DSA were used together, and it was found that the two observers using DSA, respectively, identified 61% and 18% of mild unprocessed EEG changes, 70% and 71% of

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moderate changes, and 95% of severe changes. This was limited however, as it was based on two observers. There was also a significant difference in performance between the two observers on the mild EEG change task. We can at least conclude that mild EEG changes on DSA are more difficult to detect. There have not been any similar studies looking at DSA performance in the context of CEA. For non-OR EEG interpretation, Moura et al. [86] analyzed performance by three neurophysiologists on 2094 h of EEG review, and DSA showed sensitivities of 98.7% for focal slowing and 100% for generalized slowing. Although there are differences between OR and non-OR interpretation (retrospective vs real-time interpretation; proportion of sedated patients), this shows that DSA potentially can perform as well as view unprocessed EEG for certain tasks. There are many qEEG measures under investigation in CEA. Kamitaki et al. [59] looked at many different measures (alpha, beta, theta, delta power; alpha-delta ratio; beta-delta ratio; amplitude-integrated EEG; spectral edge frequency) in 118 CEA cases and found that in patients with ischemia following clamping, all qEEG measures were found to be significantly decreased compared to post-clamp values. Although quantitative EEG is quickly growing in applications in non-OR settings, its role for monitoring CEA has not been extensively investigated. Its usefulness may depend on the interpreter’s experience in using unprocessed and quantitative EEG, as well as number of monitored cases. SSEP Monitoring SSEPs are used widely in IONM. Due to the strong correlation between SSEPs and cerebral ischemia, as discussed earlier, SSEPs are now commonly used as intraoperative surrogates for cerebral ischemia. In CEAs, the cerebrovascular territories at risk include the ipsilateral ICA, and more specifically the middle cerebral artery (MCA) territories. The anterior cerebral artery (ACA) territory tends to be less at risk than the MCA as it receives more collateral flow from the anterior communicating artery than the MCA. To monitor these territories, an appropriate neurophysiological signal that is generated from structures in these territories must be selected. The SSEP signal is generated from the somatosensory cortex in the parietal lobe. The primary hand sensory areas are included in the MCA territory and the primary leg sensory areas in the ACA territory. The median or ulnar nerve SSEP, which results in a hand sensory area cortical signal, is therefore a good marker of functional status and ischemia in the MCA territory. Compared to EEG, SSEPs are more resistant to anesthesia, require fewer electrodes, and are easier to interpret/report and easier to compare over time [79]. SSEPs have been well studied in CEA. Their use in CEA was first reported in 1982 by Moorthy et  al. [82]. Another early case series of 38 patients (28 with regional anesthesia) was Markand et al. [80], where 4 patients had SSEP changes following cross-clamping reversed by shunting. There subsequently were many studies that supported the reliability and accuracy of SSEPs in CEA [5, 45, 52, 60, 114, 132].

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The sensitivity of SSEPs was found to be 100% with a specificity of 86.5% in a study of 196 patients [97]. False negative and false negative rates were reported as relatively low in multiple studies, with the false negative rate of 0–3.5 in one review [5, 63, 78, 139]. A more recent meta-analysis of SSEP in CEA of 4557 patients showed a sensitivity of 58%, a specificity of 91%, and a false negative rate of 0.96% [91]. True positives were defined as SSEP changes with a new postoperative deficit for this review, which may lower sensitivity, as mentioned in the EEG monitoring section. Lam et al. [63] reviewed six studies and found sensitivities ranging from 83% to 100% and specificities from 83% to 99%. They also concluded that EEG and SSEP monitoring had similar sensitivity/specificity. Fisher et al. [39] performed a meta-analysis of 3028 patients and found SSEP changes in 5.6% of cases, with 20% of patients with SSEP changes developing a postoperative deficit. Though most studies have reported good performance of SSEPs, there are some studies that have raised concerns that SSEPs are not sensitive enough for cerebral ischemia and unreliably predict neurologic outcome [63, 139]. In Lam et al. [63], SSEPs were compared to EEG, and the authors reported that there was prolongation of the central conduction time in 10 of 23 patients with EEG evidence of ischemia but a SSEP amplitude reduction of >50% in only 1 of 23 patients. Based on these results, they felt that these specific criteria were not sensitive enough to detect cerebral ischemia. In Wöber et al. [139], 32 patients were evaluated, and it was found that between shunted and non-shunted patients, there were no differences in the cortical SSEP amplitudes and latencies. They also conducted a meta-analysis of 15 studies and found no improvement in neurologic outcome with selective shunting and SSEP monitoring. This meta-analysis was limited by several factors; the authors noted these to be that transient neurologic deficits may have been underestimated or not reported in some studies, possible discrepancies in data in some studies, and inclusion of multiple serial series by the same groups. Additionally, there were no uniform criteria for shunt placement between studies and there were differing definitions of critical SSEP changes. A differing view was presented in Amantini et al. [5], which concluded that EEG monitoring had a high incidence of false positives compared to SSEPs because there is less agreement on what constitutes a significant EEG changes compared to an SSEP change. Most studies have found a 50% amplitude reduction of the cortical SSEP (N19/P24), or a 1 ms delay of the central conduction time correlates best with the development of postoperative neurologic deficits [16, 25, 45, 52, 60, 61, 114]. A 50% reduction in SSEPs has also been associated with worsened performance on neuropsychological testing performed pre- and postoperatively [16]. Other than immediate postoperative deficits, there is some suggestion that SSEP and EEG changes might also predict long-term stroke. In Domenick Sridharan et  al. [31], follow-up of 853 consecutive patients showed that patients with SSEP or EEG changes compared to those without had a stroke-free survival rate of 88.2% vs 94.7% at 5 years and 78% vs 86.1% at 10 years. There was no difference in overall survival at 10 years.

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EEG and SSEP have been frequently combined for monitoring of CEA as well. Thiagarajan et al. [129] performed a meta-analysis which found that using EEG and SSEP together was 1.32 times more sensitive than EEG alone and 1.26 times more sensitive than SSEP alone. Overall, we can conclude that SSEP monitoring for CEA is a reliable modality for identifying intraoperative ischemia. MEP Monitoring Since their introduction, MEPs have quickly expanded in use in IONM and are well established for monitoring spinal surgeries. There remain more questions on their use and interpretation in cerebrovascular disorders. Many of these questions arise from the lack of similar studies regarding impact of rCBF on MEPs in comparison to literature evidence for the utility of EEG and SSEP. Despite this, there are many studies on their use for monitoring in this context. In our institution, TcMEPs are a standard part of our multimodality monitoring approach to cerebrovascular disorders. There have been several studies that have used the combination of SSEP, TcMEP, and EEG together for monitoring CEAs. The addition of TcMEPs can potentially identify pure motor subcortical ischemia, which monitoring with only SSEP and EEG would likely not detect [49]. In Malcharek et al. [73], 9 of 600 patients (1.5%) undergoing CEA were shown to have isolated transient MEP changes thought to be due to subcortical ischemia. Three of those patients developed postoperative motor deficits. In a follow-up, Malcharek et al. [74, 75] found a 0.4% false negative rate for multimodal monitoring with MEPs, with MEP changes in 32 patients (12.1%), 11 patients (4.2%) with transient motor deficits, and 1 patient (0.4%) with permanent motor deficits. Isolated motor changes were not seen in Alcantara et al. [4], with 11 of 181 patients (6%) with reported changes during IONM, all with SSEP changes and 6 also with MEP changes. Interestingly, Malcharek et al. [74, 75] compared outcomes in awake CEA versus multimodal monitoring and found similar motor outcomes (postoperative deficits of 4.9% vs 4.3%), with less technical failures (defined as not being able to record either SSEPs or MEPs for the general anesthesia group and as not being able to perform a clinical neurological evaluation in the regional anesthesia group) in the multimodal monitoring group. Overall, these studies show that the addition of MEP monitoring provides added benefit in the monitoring of CEAs. The technical setup of these studies was similar, typically sampling a hand and foot muscle bilaterally, as these areas have large cortical representation. Our institutional practice is to sample the hand (APB-FDI), tibialis anterior (TA), and adductor hallucis (AH) while primarily tracking the stimulation threshold for the hand only, and the threshold required to elicit the hand together with either the TA or AH. There is no consensus on the alarm criteria to be used in monitoring MEPs [72]. The previously mentioned studies on MEP monitoring in CEA tended to use MEP loss as their criteria, with threshold level MEP responses used.

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A large concern in using MEPs for cerebrovascular monitoring is overstimulation. As stimulation increases above threshold, the probability of directly activating deep subcortical motor pathways, and thus undercutting the cortex, increases. If this occurs, there can be false negative monitoring for cortical ischemia. SSEPs do not have the same concern, as the near-field scalp evoked potential is generated at the cortex. Using close to motor threshold stimulation minimizes the risk of this occurring [49]. It is important to ensure there is no crossover (simultaneous MEPs recorded from ipsilateral limbs) present when obtaining MEPs in this context. The presence of any ipsilateral response is a sign that deeper motor pathways are being activated. Direct cortical MEPs (dcMEPs) can potentially avoid the issue of deep subcortical stimulation but are more common when the intracranial space is already being accessed such as in cerebral aneurysm clipping. However, studies of MEPs and CEA only included utilization of TcMEPs. Malcharek et al. [76] retrospectively looked at different MEP warning criteria in 571 patients. They found that that using criteria of a 50% reduction in MEP amplitude and area under the curve resulted in false-positive rates of 24% and 29%, respectively, and concluded that using such criteria was likely not useful. Currently, based on the literature, using MEP loss is the preferred method in CEA monitoring. That amplitude criteria are not as useful in this scenario does not seem surprising. At close to threshold levels used in cerebrovascular monitoring, MEPs exhibit greater trial to trial variability than at suprathreshold levels [58]. It is possible that monitoring changes in threshold MEP level may be useful, but these have not been studied in this context yet. Overall, these studies show that the addition of MEP monitoring provides added benefit in the monitoring of CEAs.

Transcranial Doppler (TCD) Transcranial Doppler approaches cerebral ischemia from a different perspective. While EEG, SSEP, and MEPs focus on measuring cerebral function as a surrogate for ischemia, TCD focuses on measuring cerebral blood velocity and detection of embolic events. EEG and evoked potentials can miss smaller embolic events. If an embolus occurs outside of the pathway that generates the evoked potential signal, then no change will be detected as EEG is limited to the evaluation of subcortical ischemia. TCD is able to measure the blood flow velocity in large intracranial arteries like the ICA, MCA, ACA, and basilar and vertebral arteries. The technique is based on the Doppler effect. The TCD probe emits ultrasound waves which reflect off moving red blood cells. Due to the Doppler effect, the reflected waves will be of a slower frequency. The difference in emitted and reflected frequency is proportional to velocity and can be used to calculate the blood flow velocity. Blood flow velocity in turn can provide useful clinical information on intracranial vascular abnormalities. Vessel stenosis can result in an increase in blood flow velocity. Additionally, if fluctuations in arterial blood pressure and CO2 remain small, then changes in blood flow

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velocity are felt to be reflective of cerebral blood flow. A reduction in mean flow velocities or slow flow acceleration is thought to occur in the setting of hemodynamic compromise [120]. TCD is able to detect microscopic emboli, which have characteristic changes. In IONM, TCD has seen variable use and is utilized more often in specific centers. It tends to be less common than EEG or SSEP and is mostly limited to CEA.  There are several technical factors that limit more widespread use. These include lack of an adequate acoustic window in a significant number of patients; the probe becoming dislocated, as it is relatively close to the surgical field; and the requirement of personnel specifically trained in its use. Despite its limitations, TCD has been well studied in the context of monitoring CEAs. Halsey [50] conducted a multicenter, retrospective trial of 1495 patients. Ischemia was classified based on reduction in mean velocity with 16–40% of preclamp velocity classified as mild and 0–15% as severe. These cut-offs were based on other studies that correlated ischemia using EEG and rCBF [9, 57, 81, 121]. Major findings of this trial included that in patients with no evidence of ischemia (mean velocity remained >40% of baseline), the risk of stroke was higher in the shunt group than the no shunt group (4.4% vs 0.7%) and 7.2% of cases had severe ischemia. In these severe ischemia cases, ischemia resolved spontaneously in half. In patients where severe ischemia did not spontaneously resolve, the rate of stroke was high, with shunting protective against stroke. Six of 13 patients with severe ischemia and no shunt developed stroke, though 1/3 of these severe strokes were hemorrhagic stroke or carotid thrombosis. In the mild ischemia group, stroke rates were 3.9% vs 0.6% in the shunt vs no shunt groups. Bornstein et al. [12] looked at velocity changes in 50 consecutive CEA patients performed under regional anesthesia with TCD monitoring. They found that the velocity changes seen were similar in patients with and without complications and concluded that TCD was not useful in deciding whether to shunt in CEA. Another study in CEA under regional anesthesia was performed by Moritz et al. [85]. This was a study of 48 patients and compared TCD, stump pressure measurement, near-­ infrared spectroscopy, and SSEPs. They found that all techniques were able to detect ischemia; however SSEPs had the lowest accuracy. In this study, SSEPs were performed with a stimulation intensity of 10 milliamps (mA), likely to avoid patient discomfort, as the patient was awake. At this intensity level, it is unlikely that a supramaximal SSEP signal, as is usually desired, was obtained, which may explain why the SSEP performance in this study was worse. TCDs were not able to be recorded in 21% of patients due to technical difficulties. EEG, SSEP, and TCD were compared by Rowed et al. [109]. One hundred fifty-­ six patients were monitored with SSEPs and EEG, and TCD monitoring was attempted in 91 patients. TCD monitoring was only technically successful throughout the procedure in 63% of patients. EEG yielded one false negative, no false positives. SSEP had no false negatives or positives. None of the TCD emboli detections were associated with postoperative deficits. A larger recent meta-analysis looked at TCD monitoring in 4705 patients [134]. They found that TCD monitoring of cerebral microembolic signals and MCA

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velocity yielded a sensitivity of 56.1% and a specificity of 72.7% for perioperative stroke. MCA velocity changes alone had a sensitivity of 49.7% and specificity of 84.1%. The authors stated they did not find studies where TCD was combined with SSEP and EEG, so they were not able to perform a comparison. A limitation of this study is the pooled studies used differing standards for critical MCA velocity or microembolic signal changes, as there is no agreed upon critical value. Overall, TCDs do show utility in monitoring CEA but are more limited compared to other modalities due to technical difficulties and due to the ability to only monitor one intracranial vessel. There have not been many studies comparing them directly to SSEP or EEG, but in the existing studies, it did not clearly appear to be superior.

Near-Infrared Spectroscopy (NIRS) NIRS, sometimes referred to as cerebral oximetry, is a noninvasive technique for assessing cerebral oxygenation. The technique depends on light in the near-infrared range to evaluate cerebral oxygenation [120]. Beer-Lambert law states that the amount of light transmission through a solution is a function of the concentration of the absorbing molecules in the solution and the length of the path [135]. Oxygenated and deoxygenated blood have characteristic and distinct absorbance spectra [24]. By using this characteristic of oxygenated blood, it is possible to use near-infrared light to determine the level of oxygenated blood cerebrally. Additionally, an advantage of the near-infrared spectrum of light is that skin, skull, and other biological tissue are relatively transparent to this wavelength. This allows blood in the brain to be analyzed. There are a number of commercially available cerebral oximeters available for use in the United States presently. These include the INVOS (Somanetics/Covidien, Boulder, CO), ForeSight (CAS Medical Systems, Branford, CN), EQUANOX (Nonin Medical, Plymouth, MN), CerOx (Ornim Medical, Lod, Israel), NIRO (Hamamatsu Photonics, Hamamatsu City, Japan), TOS-96 (Tostec, Tokyo, Japan), and Root with O3 Regional Oximetry (Masimo, Irvine, CA). These devices work by measuring the ratio of hemoglobin to oxyhemoglobin using a single light-emitting diode with near-infrared light transmitted with a wavelength of 724 and 810 nm and recorded with two photodiodes [24]. One can refer to the excellent reviews by Wahr et al. [135] and Davies and Janelle [24] for a more detailed review of the technology underlying cerebral oximetry, which is beyond the scope of this chapter. There have been many studies looking at the performance of NIRS in CEA. As mentioned in the previous section, Moritz et al. [85] compared NIRS, TCD, EEG, and SSEP in CEA under regional anesthesia and found that all of the techniques were able to identify cerebral ischemia but that NIRS and stump pressure measurement had the highest accuracy, as compared to clinical deterioration which was

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described as the gold standard. Clinical deterioration was defined as any new neurologic deficit occurring, such as speech abnormalities, motor weakness, or impaired consciousness. The patient’s clinical exam was assessed every 30 s during surgery, with orientation, command following, and handgrip assessed by the anesthetist. In Beese et al. [10], NIRS and SSEP were compared in 317 CEA patients. SSEPs were stable in 287 of 317 patients, and none of these patients developed postoperative deficits. Twenty-seven of 317 patients (9%) had flattening of the SSEP during cross-­ clamping. These patients had the regional cerebral saturation (rSO2) before cross-­ clamping and the trough level after cross-clamping recorded. It was found that a statistically significant decrease of rSO2 was seen in patients both with (65.8% vs 56.1%) and without (63.9% vs 60.9%) SSEP changes. Substantial interindividual variability and change of rSO2 did not allow them to define a threshold value. From this they concluded that without a threshold rSO2 value for cerebral ischemia, interventions based on cerebral oximetry were not justified. Rigamonti et al. [106] attempted to establish a threshold in a prospective study of 50 CEA patients with regional anesthesia. They monitored clinical signs, EEG, and NIRS. Patients who had clinical or EEG changes and required shunt showed a 16% decrease in rSO2 vs 8% in non-shunted patients (p = .01). A decrease of 15% in rSO2 had an odds ratio of 20 for severe cerebral ischemia. The same decrease of 15% had a sensitivity of 55% and specificity of 82%. The authors concluded that although NIRS could correlate with cerebral ischemia, they were not able to identify a threshold that could be used alone for prediction of shunt placement due to poor sensitivity and specificity. A literature review by Pennekamp et al. [98] had similar conclusions that, although NIRS correlated with TCD and EEG, a threshold was unable to be determined for selective shunting or cerebral ischemia. Poor sensitivity and specificity were similarly seen in a more recent meta-­ analysis of 1237 NIRS in CEA under regional anesthesia [33]. In that study, summary sensitivity was found to be 72% with a specificity of 84.1%. The authors concluded that NIRS could not be used alone to monitor CEA under regional anesthesia, and the threshold for ischemia remains poorly defined. In that metaanalysis, 8 of the 11 studies reported a relative decrease of around 15–20%. A Cochrane review of NIRS for perioperative monitoring (including non-CEA surgeries) concluded that it was unclear whether NIRS had an effect on postoperative stroke due to wide confidence intervals and a low number of events in published studies [140]. The technical setup of NIRS is relatively straightforward compared to other monitoring modalities, similar to applying pulse oximetry. Some of technical factors that can affect its signals include lack of correlation and agreement between different NIRS devices, vulnerability to light and movement artifacts (such as overhead surgical lights), and the ability to only detect regional oxygenation (usually in the frontal lobes, as this is the hair follicle-free skin area that overlies the brain) [115]. NIRS should probably not be used as the sole modality for monitoring CEA. Its exact role in CEA monitoring is not completely clear.

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Monitoring Intracranial Cerebrovascular Disorders The rationale and basis of IONM for CEA also translates similarly to intracranial cerebrovascular disorders. IONM may be useful in patients undergoing surgical or endovascular treatment of cerebral aneurysms, cerebral arteriovenous malformations (AVMs), cerebral cavernous malformations, intracranial vascular occlusive disorders, and deliberate cerebral vessel occlusion.

Cerebral Aneurysm Surgery Due to the strong correlation between SSEPs and cerebral ischemia seen experimentally, these modalities naturally became adopted for the monitoring of cerebral aneurysm surgery. Besides being able to monitor for cortical ischemia, SSEPs also are able to provide functional information about the integrity of the cortical and subcortical somatosensory pathways. This is an advantage over EEG, which also provides information on cortical structures. In intracranial non-epilepsy surgery, EEG is more limited in its use of detecting cerebral ischemia as EEG recording is interfered with by the introduction of airspace between the dura and arachnoid mater that occur from craniotomy and brain relaxation [35]. It has been shown that median nerve SSEPs also provide information on thalamic activity supplied by the posterior cerebral artery [17]. As previously mentioned, the cortical generator of the median or ulnar nerve SSEP lies in the parietal cortex in primary sensory cortex representing the hand, located in the MCA territory, while the cortical generator of the posterior tibial nerve SSEP lies parasagitally in the primary sensory cortex, in the ACA territory. Our typical setup for aneurysm and AVM surgery varies depending on the cerebrovascular territory that is felt to be most at risk. We will include EEG, median/ ulnar nerve SSEP, posterior tibial nerve SSEP, and TcMEPs (sampling the hand (FDI-APB), TA, AH) for all territories. For vertebrobasilar cases we will include BAEPs and sometimes free-running cranial nerve EMG. For ACA territory procedures, we will include additional centrally located stimulation electrodes (e.g., at Cz) to better isolate leg MEP responses. Earlier studies of IONM in aneurysm surgery involve a combination of EEG, SSEP, and BAEP. Palatinsky et al. [93] reported the outcomes of ten studies of MCA aneurysm and found median nerve SSEPs were 78–100% reliable in predicting clinical outcome. Friedman et  al. [43] found a decrease or disappearance in the cortical SSEP accurately predicted postoperative deficits. In López et al. [71], 70 aneurysm cases monitored with SSEP, EEG, and or BAEP were evaluated. The authors found that 26% of patients had transient SSEP changes and 4% with transient BAEP changes. Aneurysm clip placement caused IONM changes in 9 of 70 cases, with removal or adjustment of the clip resolving changes in all cases. Other changes were caused by transient hypotension and retractors. Two patients had

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persistent IONM changes, one developed a new deficit post-op, and one died. Manninen et  al. [77] reported SSEP and BAEP use in posterior fossa aneurysm surgery. They found that 10 of 67 patients showed BAEP changes, with 6 developing a postoperative neurologic deficit. The false negative rate of SSEP/BAEP was 20%. Friedman et al. [42] reported the results of 53 patients undergoing MCA aneurysm surgery. New postoperative deficits were seen in four patients with persistent SSEP changes, while one of five patients with a transient SSEP change developed a postoperative deficit. There was one false negative case. SSEPs were also able to identify a case of peripheral ischemia in this series, as in one patient a malfunctioning blood pressure cuff caused limb ischemia. Schramm et al. [113] looked at 134 aneurysm cases and found alteration of surgical course in 15 of 17 instances of SSEP changes. Using multimodality monitoring can be useful in identifying focal or regional ischemia, which is of importance in intracranial aneurysm surgery, where the vascular territories involved are more variable compared to those in carotid surgery. Multimodal monitoring has been reported in an increasing number of studies in cerebral aneurysm surgery. Quiñones-Hinojosa et al. [102] reported a series of 30 patients undergoing basilar artery aneurysm clipping performed with monitoring of SSEP, EEG, and MEP.  Changes occurred in 10 of 30 patients, with 6 caused by temporary clipping, 3 by permanent clipping, and 1 by retraction. Isolated TcMEP changes occurred in five patients, with four patients having changes in both TcMEPs and SSEPs and a single patient with isolated SSEP changes. All changes were transient after corrective measures. They felt that the results suggested that TcMEPs may be more sensitive than SSEPs for basilar artery procedures. Horiuchi et al. [54] looked at dcMEPs and SSEPs in MCA aneurysm surgery in 53 patients. Nine patients had transient dcMEP changes, with five of those being isolated MEP changes of which three had transient motor deficits. One patient had persistent dcMEP loss and developed postoperative hemiparesis, with imaging showing a subcortical infarct. Sasaki et al. [111] analyzed cerebral infarction of perforating artery territories in 1043 patients who had underwent aneurysm surgery. They found that intraoperative microscopic inspection was not able to determine the patency of perforating arteries, but MEPs were able to detect disturbances in blood flow in several perforating arteries (anterior choroidal artery, lenticulostriate arteries), whereas SSEPs were less useful for this purpose. Infarct was related to aneurysmal neck clipping, temporary occlusion of the parent artery, direct injury, retraction, and trapping of the parent artery. Similarly, Neuloh and Schramm [88] also found that TcMEPs were better than other modalities at detecting subcortical ischemia. There are now several large studies reviewing the performance of different IONM modalities in aneurysmal surgery. In Thirumala et  al. [130, 131], a meta-­ analysis of 2015 patients was performed. They found that SSEP changes had a sensitivity of 56.8% and a specificity of 84.5%. SSEP sensitivity may be lower here, as the analysis included anterior and posterior circulation aneurysms. In general, SSEPs appear less sensitive to brainstem infarcts. Sahaya et al. [110] reported their

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experience with 470 procedures with SSEP and EEG in endovascular and surgical aneurysm repair. They found that IONM changes demonstrated a sensitivity of 90%, a specificity of 98%, and a negative predictive value of 99.78%. For multimodal monitoring, a systematic review and meta-analysis by Zhu et al. [142] looked at SSEP and MEP in 4011 patients in 35 studies. The pooled sensitivity and specificity were as follows: SSEP 59% and 86%; MEP 81% and 90%; and MEP and SSEP 92% and 88%. The analysis was limited by modest quality and high heterogeneity of the primary studies. Park et al. [95] compared aneurysm clipping with and without IONM (MEP/SSEP) in 545 procedures. Procedures without IONM all occurred prior to procedures with IONM in this study. IONM changes had a sensitivity of 90%, a specificity of 94%, and a negative predictive value of 99.7%. The rate of postoperative neurologic deficits in the non-IONM group was 6.7% compared to 3.1% in the group with IONM.  Additionally, patients with IONM had lower rates of sustained postoperative neurologic deficits (odds ratio = 0.36), ischemic complications (odds ratio  =  0.39), and radiologic complications (odds ratio  =  0.4). Overall, from these studies, we can see that using a multimodality IONM approach effectively identifies cerebral and brainstem ischemia.

Cerebral AVMs The number of studies on the use of IONM in monitoring AVM surgery is much less than that of aneurysms but also supports the use of IONM in this context. Chang et al. [18] looked at 56 cases of vascular malformation resection. SSEPs were monitored in 96% of these cases and BAEPs in 30%. Five of 54 patients (9%) had SSEP changes, with 4 patients with transient changes and 4 patients who developed new transient postoperative deficits. In those patients with transient SSEP changes, adjustment or removal of clips or increasing MAP resolved the changes. There were one false negative in the BAEP group and one change with associated permanent deficit. The overall sensitivity for SSEP and BAEP was 86% and specificity was 98%. Ichikawa et al. [55] also described the use of MEPs in AVM resection in a series of 21 patients. Selected patients had lesions where motor cortex or corticospinal pathways were felt to be directly at-risk during resection. Either dcMEPs or TcMEPs were used, with dcMEPs used if motor cortex was exposed. The warning criteria consisted of MEP disappearance and/or a decrease in amplitude of 50% or more. Five of 21 patients showed MEP changes, with 4 transient changes and 1 persistent loss. Two of these patients developed transient motor deficits and two developed permanent motor deficits. Causes of changes included temporary occlusion of a feeding artery, venous infarction, coagulation of a capillary network, and AVM bleeding. The authors felt that monitoring using MEP was useful in differentiating passing arteries from feeding arteries.

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Extracranial-Intracranial (EC-IC) Bypass The goal of EC-IC bypass surgery is revascularization and involves taking an extracranial artery branch and anastomosing it into the intracranial vasculature, bypassing a stenotic or occluded proximal vessel. The most common EC-IC bypass is the superior temporal artery-middle cerebral artery (STA-MCA) bypass. EC-IC bypass has been used to treat a variety of conditions: moyamoya disease, symptomatic vascular stenosis, aneurysm, and tumors requiring vascular sacrifice [105]. In STA-­ MCA bypass, the STA is grafted to a branch of the MCA. While anastomosis of the STA to the MCA is occurring, the MCA must be occluded, and there is a risk of cerebral ischemia. In what appears to be the only published study on IONM in EC-IC bypass, Dengler et al. [27] described the use of TcMEP monitoring in EC-IC bypass in 32 cases with SSEP used as a backup if TcMEPs were not able to be monitored. They observed 14 reversible TcMEP changes, with 1 patient developing a transient postoperative deficit, and 1 irreversible TcMEP change associated with a permanent neurologic deficit. Reasons for reversible changes included temporary occlusion of the recipient vessel (leading to a more distal bypass site being chosen), the occurrence of bypass anastomosis (reversed with MAP increase or after anastomosis is complete), temporary aneurysm clipping (leading to repositioning of the clip), and others. There were no false negative events. Warning criteria used in this study were a reduction of TcMEP amplitude of more than 50% or an increase of TcMEP peak latency >10%. MEPs were obtained at a near-threshold level. The use of 50% amplitude reduction criteria might explain the relatively high number of changes in this study (15 of 32 cases). In our institution, the practice is typically to obtain near-­ threshold MEPs and use an 80% reduction in MEP amplitude as warning criteria. As detailed in the section on MEP monitoring in CEAs, variability of MEPs at near-­ threshold levels may make following complete MEP loss a preferable warning criterion in cerebrovascular monitoring. Due to this risk of cerebral ischemia, IONM can potentially play a role in monitoring these surgeries, using a combination of EEG, SSEP, and MEP.

Interventional Neuroradiologic Procedures Interventional neuroradiologic (INR) procedures have rapidly expanded in volume and are now a routine occurrence in many institutions. Diseases previously treated surgically can now often be treated endovascularly. The potential risk of cerebral ischemia present in open surgical cerebrovascular cases remains in endovascular procedures. The use of IONM in these procedures has grown, as evidenced by an increase in the number of reports on IONM in INR procedures in the last decade. EEG, MEP, SSEP, and BAEP can equally be applied in the endovascular suite to monitor selected procedures. The most common of these include carotid artery

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angioplasty, deliberate arterial occlusion of extra- and intracranial arteries, coiling of cerebral aneurysms, placement of flow-diverting stents for aneurysms, and glue embolization of cerebral AVMs. The exact modalities chosen to monitor these procedures depend on the cerebrovascular territory that will be at risk and whether the patient will be under general anesthesia or awake during the procedure. The IONM setup and recording for INR procedures is similar to surgical cases. There are a few small differences. We do not use corkscrew EEG electrodes, as the artifact associated with these can obscure imaging. For patients being stented and on dual antiplatelet therapy, we use cup electrodes rather than needle electrodes, as we have observed cases of extensive subdermal hematoma with needle electrodes. Paulsen et  al. [96] reported using SSEPs in 23 rolandic AVM embolizations. During amobarbital sodium testing, one awake case showed a SSEP change with associated transient neurologic deficit, and a second general anesthesia case showed a SSEP change. The authors felt that SSEPs and clinical neurological examination were useful tools in this context. Paiva et al. [92] used EEG monitoring in AVM embolization and found focal or diffuse low-frequency abnormalities were followed by clinical hazards in 3 of 11 cases. Positive amobarbital testing in this study caused ipsilateral focal slowing. Liu et al. [68] also report the use of IONM in 35 patients, with management altered in 5 of 35 patients. Dietz et al. [30] looked at 17 patients undergoing balloon test occlusion of the ICA (due to tumor infiltrating the area). These patients were monitored using clinical exam, SSEP, TcMEPs, and TCDs. Balloon test occlusion is performed when a vessel, such as the ICA, needs to be sacrificed. It involves temporarily inflating a balloon in the ICA and looking for changes in the patient’s neurological exam or neurophysiologic indices to determine if the vessel can be safely sacrificed. Their conclusion was monitoring was important in predicting outcome from permanent occlusion of the ICA. Cloughesy et al. [23] used clinical exam, EEG, and qEEG for monitoring balloon test occlusions. They found 4 of 17 cases with changes. These changes were as follows: increased slowing and clinical changes; attenuation of the alpha band, but no clinical change; and clinical change without EEG change. More recently, Takamura et al. [127] compared the performance of preoperative balloon test occlusion done awake with intraoperative findings. Patients underwent a standard balloon test occlusion prior to their surgery. The systolic blood pressure was kept under 140  mmHg, and tests were considered negative if there were no changes after 20 min of occlusion. During this period, patients underwent continuous neurological evaluation, not further specified in the study. The majority of surgeries following balloon test occlusion were CEAs (28 of 32). Any change during cross-clamping was noted. The accuracy of multimodality monitoring was compared to BTO. MEPs were performed at an intensity of 20% higher than threshold level. They found that a >80% amplitude reduction in MEPs resulted in a sensitivity and specificity of 100% for a positive balloon test occlusion. They found that in this comparison MEPs performed better than EEG and SSEP in accuracy. This study is similar to studies comparing modalities in CEA done under regional anesthesia, but the clinical exam for balloon test occlusion may be more accurate, as the patient is on minimal anesthetics for balloon test occlusion compared to CEA.

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Pandey et al. [94] looked at the use of BAEP in six patients undergoing vertebrobasilar stenting and angioplasty. They found that one patient had a 1 ms increase in wave V latency during angioplasty, and the patient developed post-procedural hemiplegia. There have now been several larger studies on the use of IONM in INR. Phillips et al. [100] looked at 873 patients undergoing INR procedures who were monitored with SSEP. They found 52 of 873 patients with SSEP changes. Twenty-four of these were reversible and 28 patients had persistent changes. The negative predictive value of reversible SSEP changes for postoperative stroke was 83%. It does not appear there was false negative SSEP monitoring. Sensitivity and specificity of unstratified SSEP changes were not calculated. Ares et al. [7] looked at 888 cases of SSEP monitoring in endovascular aneurysm cases. They found SSEP changes occurred in 8.6% of cases with 3.1% of patients developing new postoperative deficits. A transient or persistent total loss of SSEP had an odds ratio of 267 for development of a new deficit. A 50–99% loss in SSEP amplitude was associated with an odds ratio of 18.4 for a new deficit. False negative rate, sensitivity, nor specificity was specifically reported. Lee et al. [64] reported SSEP and MEP monitoring in 578 patients undergoing INR procedures. SSEP changes occurred in 1% of patients, and MEP changes in 1.2%. Postoperative deficits developed in 0.7% of patients. They determined a sensitivity and specificity of SSEPs to be 100%, and 50% and 99.5% for MEPs. The sensitivity and specificity in this study were limited by the occurrence of relatively few postoperative deficits. Similar performance is seen for IONM in AVM embolization. Church et al. [22] looked at 173 embolizations monitored with SSEP and EEG and found a negative predictive value of 90%. They also noted that their overall complication rate (1.3%) was among the lowest reported in the literature for this indication, which suggests IONM may improve outcomes. In a large study, Wilent et al. [138] analyzed 2278 INR cases where SSEP, MEP, and EEG monitoring were used. Seven hundred and sixty-three of the 2278 cases used MEPs; the rest did not. They had an overall incidence of postoperative deficit of 1.2%. In cases with IONM changes, 20% of these patients developed a deficit, while 0.09% of cases without a change developed a deficit. Complete signal loss had an odds ratio of 1437 for a postoperative deficit. Cases with MEP monitoring had a sensitivity of 92.3% compared to 85.7% without, and a specificity of 96.7% vs 98.2%. There are many studies that support the use of multimodality IONM in interventional neuroradiologic procedures. In addition to monitoring procedures, provocative testing can also be performed. At our institution, endovascular treatment of AVMs typically involves provocative testing. This involves superselective intra-arterial injection of an agent, usually 50 mg of amobarbital sodium (methohexital, propofol, pentobarbital, and etomidate have also been described) into the pedicle that will be embolized or the vessel that will be embolized. If there is a significant change in the patient’s EEG, evoked potentials, or clinical exam, this suggests that the vessel likely supplies blood flow to normal cerebral tissue and should not be embolized. Instead, a different or more distal vessel can be tested. If no change occurs, then embolization will proceed.

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Bican et al. [11] detail the use of provocative testing in awake patients and patients under general anesthesia. This was a series of 63 cases, with 9 awake and the rest under general anesthesia. There were no instances of new neurologic deficits. Provocative testing was positive in two patients and results were comparable between general anesthesia and awake groups. Specificity of testing was reported as 100%. Provocative testing can also be used for spinal lesions, such as spinal dural arteriovenous fistulas; this will be covered in the chapter on monitoring spinal cord ischemia. There are relatively few studies on how IONM affects cost. Feng et  al. [37] looked at patients undergoing AVM embolization in a large database. They found that in patients who underwent embolization with IONM, length of stay was shorter (2.72 vs 4.92 days), complication rates were lower (0% vs 1.88%), and total payment was lower (40,179$ vs 50,844$). As with database studies, there may be many potential confounders in these results, such as hospitals with IONM services for embolization being more likely to be larger centers with more experience. Mechanical Thrombectomy for Acute Stroke In the last decade, mechanical thrombectomy for the treatment of large vessel occlusions in acute stroke has gone from experimental to standard of care [3, 41, 46, 47, 89]. Mechanical thrombectomy is an interventional neuroradiologic procedure where an acute thrombus of a large cerebral blood vessel, most often the ICA or M1 segment of the MCA, is removed with a stent-retriever device. With this type of treatment, many patients are able to walk away from previously devastating strokes with minimal deficits. In SWIFT PRIME 60% of patients receiving thrombectomy had a 90-day modified Rankin score (mRS) of 0–2 vs 35% of the control group [112]. While it is not the current practice at our institution to monitor mechanical thrombectomy, there are other centers where it is common. The ideal IONM setup for these procedures is not clear yet. Greve et al. [48] employed a single modality, MEPs recorded at the bilateral adductor pollicis brevis. Only monitoring MEPs may provide an advantage in decreased setup time and may be appropriate if the goal is to only provide prognostic information. Compared to other procedures, shorter setup time is more important in thrombectomy. The American Heart Association stroke center goals for thrombectomy are a door-to-­ device time in 50% of transfer patients of 60 and 90  min in directly arriving patients, door being defined as arrival into the hospital [6]. Another logistical concern is that many of these procedures are performed under moderate sedation, which may limit the use of needle electrodes and further increase setup time. Additionally, if the patient is not deeply sedated, it may be possible to follow the clinical exam instead. There is not yet much literature on the use of IONM in mechanical thrombectomy. The use of IONM in thrombectomy differs from many other procedures in that the neurologic deficit has already occurred prior to the start of monitoring.

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Greve et al. [48] showed that when MEP recovery occurred, it did so at a median time of 4.5 min following successful thrombectomy. Sensitivity for clinical improvement and absence of ischemia on MRI compared to modified thrombolysis in cerebral infarction (mTICI) grading 2b reperfusion (partial filling of more than 50% of the vascular territory) was slightly lower, but specificity was much higher. Shiban et al. [118] monitored SSEPs and TcMEPs continuously during thrombectomy in 20 patients. SSEPs were only technically successful in 9 of 20 cases, and MEPs 19 of 20 cases. They found that for functional outcome MEPs had a positive predictive value of 92%, SSEPs 83%, and recanalization 75%. The authors stated that a limitation of their study was that they had a small number of patients successfully enrolled as they were not able to start monitoring without causing a delay in endovascular intervention in several cases. Dickey et al. [29] showed that the interhemispheric difference in the delta-alpha ratio in qEEG following thrombectomy correlated with discharge and follow-up outcomes. Though this study was not performed in the intraoperative setting, it seems reasonable to expect similar results intraoperatively. NIRS is another modality that has been reported in thrombectomy [53, 107, 108]. Hiramatsu et al. [53] showed that interhemispheric rSO2 was shown to improve following recanalization in two patients with large vessel occlusions. Ritzenthaler et al. [108] looked at 17 patients and found that rSO2 changes did not correlate with outcome. In this context, NIRS appears to be of mixed or poor value. Overall, these studies show that IONM could provide some prognostic information. This information could potentially guide post-procedural management. One such scenario could be where MEPs show no recovery despite adequate angiographic reperfusion, suggesting completed infarct. Such a patient might merit closer post-procedural clinical monitoring. In the converse scenario, recovery of MEPs despite no radiographic flow suggests reliance on collaterals, which may be useful clinical information. Whether IONM improves neurologic outcomes for mechanical thrombectomy has yet to be studied, and the exact role of IONM in mechanical thrombectomy remains to be determined.

Definition of Critical Changes Criteria for critical changes can vary depending on the interpretation of the literature. Assuming that generalized effects such as anesthesia or technical factors have already been ruled out, we defined the following as critical changes: new focal slowing on the EEG; 50% or more reduction in the amplitude of the cortical SSEP; an increase of 1 ms or more of the central conduction time of the SSEP; loss of wave III or V of the BAEP; a 1 ms or more prolongation of wave V of the BAEP; 80% amplitude reduction in the MEP; and any alteration in the clinical neurological examination from the patient’s pre-testing baseline examination following amobarbital sodium testing.

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Possible Interventions in Response to Critical Changes In most scenarios, after IONM changes occur, the surgical or procedural management of the case is altered. It is important to emphasize that altering operative management in response to IONM changes is a fundamental reason for using IONM. Below we list some of the strategies that can be used upon encountering changes in commonly performed procedures. • Endovascular Cases –– AVMs

1. Retest the same vessel. 2. Retest a different or more distal vessel. 3. Increase MAP to increase cerebral perfusion. –– Balloon Test Occlusion



1. Deflate the balloon and retest at a different segment of the vessel for transient changes. 2. Deflate the balloon and stop testing if there are persistent changes, as this indicates permanent occlusion would likely cause a neurologic deficit.

• Cerebrovascular Disorders –– Aneurysm

1. Increase MAP but only if that does not increase the risk of hemorrhage, to increase cerebral perfusion. 2. Adjust or remove cerebral retractors. 3. Reposition or remove temporary clip(s). 4. Reposition or remove permanent clip(s). –– AVMs



1. Increase MAP to increase cerebral perfusion, again, as long as it does not increase the risk of hemorrhage. 2. Adjust or remove cerebral retractors. 3. Reposition or remove temporary clip(s). 4. Reposition or remove permanent clip(s). –– CEAs



1. Increase MAP to increase cerebral perfusion. 2. Carotid shunting. –– EC-IC Bypass



1. Increase MAP to increase cerebral perfusion.

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Stimulating and Recording Techniques There are a variety of different stimulation and recording protocols that exist for obtaining evoked potentials. A full discussion of these is beyond the scope of this chapter; however, in this section we will detail the parameters used at our institution, which we have found produce consistent and reproducible BAEPs, MEPs, and SSEPs. In general, recordings should start as early as possible in the procedure. We typically begin placement of electrodes following anesthetic induction. The initial baseline recording should be obtained prior to the initial incision and continued at regular intervals throughout the procedure. It is important to regularly obtain recordings throughout the procedure, including during lower risk portions. Doing so ensures anesthetic fade and other such factors will be accounted for. Additionally, neural injury may still occur during lower risk times. The anesthetic levels, temperature, mean arterial pressure, and surgical events should be regularly documented. During the critical portions of the procedure, it is important to continuously obtain recordings and perform TcMEPs more frequently. The vascular territory at higher risk should be sampled more frequently during the critical portion of the procedure (e.g., running median nerve SSEPs at a ratio of 3:1 with posterior tibial nerve SSEPs during temporary MCA occlusion). Monitoring should continue until the patient is awake, or as close as possible to this, as ischemia can occur during wound closure as well.

Stimulation 1. SSEPs are usually recorded after bilateral, independent median nerve stimulation. The ulnar nerve is also acceptable if the median nerve is not accessible. Standard surface stimulating electrodes are placed at the wrist. The stimulation rate is set at 2–5 Hz, with a pulse duration of 100–300 μs. The current intensity is set to a minimum level of constant current intensity that is approximately 50% above the threshold level that produces a thumb twitch. The ground electrode should be placed on the arm proximal to the stimulating electrode. Usually 150–250 stimulations are averaged, which result in reproducible and interpretable signals. 2. BAEPs are obtained after bilateral, independent ear stimulation, using ear inserts. It is preferred to use clicks with an alternating or rarefaction polarity as the stimulus. The stimulation rate is typically between 9.7 and 11.7 Hz. It usually takes 500–100 stimulations to produce an average that is reproducible and has the expected components. 3. TcMEPs are obtained ideally with activation of each hemisphere independently and sequentially. They can be elicited using standard surface EEG, subdermal

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needle, or corkscrew electrodes on the scalp. The most commonly used montages include C3–C4 and C1–C2. C3–Cz or C4–Cz can also be used and may be useful in obtaining leg responses. The near-threshold levels required to obtain the hand as well as the combined hand and leg response should be used. As discussed earlier, if stimulation levels are too high, subcortical structures can be activated, bypassing cortical ischemia.





(a) TcMEPs depend on anodal stimulation. The anode is set at the hemisphere of interest, with myogenic MEPs obtained from the contralateral limbs. For example, we would expect responses from the right body, if the anode was set at C3 and the cathode at C4. (b) The exact stimulation parameters can vary. Typical settings that will usually result in reproducible TcMEPs include pulse duration of 50–75 μs, a stimulus train of 3–7, interstimulus interval of 1.5–4.5 ms, and a maximum intensity of 500 V. The exact settings will vary widely between patients and need to be individually established. (c) Direct cortical MEPs are another method of obtaining MEPs; however the technical setup for this is beyond the scope of this chapter.

Recording Recordings of signals can be performed with a variety of electrodes. Standard surface EEG and subdermal needle electrodes are commonly employed. If surface electrodes are used, it is recommended to attach them with collodion to reduce the risk of accidental detachment. Electrode impedance should be checked when obtaining baselines and should be less than 5000 ohms during the procedure. SSEPs Electrodes should be placed on the scalp at C3′, C4′, Cz, Cz′, and Fz. In the 10–20 international electrode placement system, prime electrode sites, such as C3′, are located 2  cm posterior to their corresponding non-prime electrode positions. Electrodes should also be placed at a subcortical location and at a peripheral location (Erb’s point, popliteal fossa). Filters should be set at 30 Hz and 3 kHz. Median Nerve SSEP Suggested Montages (a) C3′/C4′–Fz (contralateral cortex to midfrontal reference). (b) C3′–C4′ (contralateral cortex to ipsilateral cortex). This may also record near-­ field cortical SSEP components (N19, P24, P40, N45).

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(c) Cervical spine (typically C5 or C7) to Fz. This can help to identify subcortical far-field potentials (P14, N18) and allows monitoring of the central conduction time (interval between P14 and N19). The CCT represents the conduction time between the foramen magnum and somatosensory cortex. (d) Ipsilateral Erb’s point to contralateral Erb’s point. This allows monitoring of a peripheral response from the brachial plexus. Posterior Tibial Nerve SSEP Suggested Montage (a) Cz–Fz (b) Cz′–Fz (c) C5/C7–Fz (d) Ipsilateral popliteal fossa to knee reference BAEPs Scalp electrodes should be placed similarly as in the SSEP section. Additionally, electrodes are placed on both ears (A1 and A2). EEG A minimum of eight channels are recommended, with four electrodes over each hemisphere. At our institution we typically use a referential montage, for example, F3/F4–Fz, C3/C4–Fz, P3/P4–Fz, and T3/T4–Fz. Additionally, occipital electrodes at O1 and O2 may be useful as well if the posterior cerebral artery territory is at risk. TcMEPs Recording of myogenic MEPs can be performed using surface or subdermal needle electrodes. It is our practice to use needle electrodes. Compared to surface electrodes, they are easy to place and relatively secure and require no electrode contact gel. Additionally, for superficial muscles, the needle may end up in the muscle, effectively becoming intramuscular recording needles. Our typical practice for cerebrovascular cases is to place paired recording needles in the hand, tibialis anterior, and abductor hallucis. In the hand we will place one needle in the APB and the other needle in the FDI. The low-frequency filter is set to 5 Hz and the high frequency filter to 2000 Hz, with a gain of 50–1000 μV/division and a sweep of 10–20 ms/ division.

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Conclusion IONM is a dynamic and evolving field within clinical neurophysiology. It has expanded greatly in scope since its inception and continues to find new uses. Applying IONM techniques in the surgical and endovascular treatment of cerebrovascular disorders requires detailed knowledge of neurology, clinical neurophysiology, neuroanatomy, neuroanesthesia, and neurosurgery. As this chapter has shown, mastering and applying IONM techniques and concepts for cerebrovascular disorders allows for the detection of cerebral ischemia and alterations in surgical and endovascular management, which may lead to improved patient outcomes. There is an ever-increasing evidence base which supports the use of IONM in a variety of procedures for cerebrovascular disorders. The field still requires additional prospective controlled trials and rigorous outcome studies to further expand the evidence base. However, finding an ethical method of doing this and not placing patients at risk for injury is a difficult dilemma, especially given our knowledge and the experimental evidence of the physiologic changes that lead to EEG and/or evoked potential changes. Subjecting patients to the high likelihood of reversible brain ischemia for the purpose of a randomized controlled trial can be argued as being unethical.

Case Examples Case Example 1 This case demonstrates some of the potential changes that can develop during CEA. An 80-year-old man with vascular risk factors is hospitalized with urosepsis and clinically develops right MCA syndrome, which improves with normalization of his blood pressure. A computed tomography angiogram (CTA) was performed (Fig. 28.2) which showed 60–70% right ICA stenosis. SSEPs and MEPs were monitored during the CEA. In the left median nerve SSEP (Fig. 28.3), we see that following a propofol bolus (surgeon preference for neuroprotection), the signal, which was originally double-troughed, simplifies in morphology, becoming single-troughed. The right median nerve SSEP shows some morphology change following the propofol bolus as well. Following carotid cross-clamping, indicated by traces following the red trace, the left median nerve SSEP initially drops in amplitude but quickly recovers in a few traces. As the signal recovered quickly without any intervention, surgery proceeded without a shunt. Approaching around 30 min of clamp time, the latency of the left median nerve SSEP begins to prolong. Around the same time, the left hand (APB-FDI) MEP (Fig. 28.4), originally obtained at a threshold level of 72  V, is no longer obtainable at 152  V.  The MAP is increased to 100  mmHg. Following this, the hand MEP re-emerges initially at a higher than baseline voltage but subsequently at the baseline stimulation level. The carotid is unclamped and, in the following trace, the left median SSEP returns to its baseline double-troughed

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Fig. 28.2  Case Example 1: Curved reformatted CT angiogram of the head and neck shows 60–70% right ICA stenosis. Hyperdense carotid plaque is seen at the carotid bifurcation

Fig. 28.3  Case Example 1: From left to right, the cortical left median nerve SSEP, right median nerve SSEP, left posterior tibial nerve SSEP, and right posterior tibial nerve SSEP are shown. The traces are shown in chronological order, with the earliest traces at the top. The vertical spacing of the traces is organized by time. A time marker is placed on the initial latency of the N20 response. Arrows show when a propofol bolus is given and when carotid clamping and unclamping occur

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Fig. 28.4  Case Example 1: MEP traces from the left hand (APB-FDI), TA, and AH are shown. Traces are shown in chronological order, with the earliest traces appearing at the top. The vertical spacing of the traces is arbitrary, and not proportional to time, as it was in the previous figure. The hand MEP is elicited at a threshold of 72 V at baseline. Following the red trace, the hand MEP is not elicitable at stimulation intensities of 152 and 192 V. Re-emergence of the hand MEP is seen at 92 V after the MAP is raised to 100. The hand MEP threshold lowers back to the baseline of 72 V once the carotid is unclamped at the second to last trace

morphology. Removal of the cross-clamp occurs just prior to the last MEP trace shown. No shunt was placed following MEP loss, as the surgeon was completing the carotid patch already. The patient awakened from surgery with no new neurologic deficits. In Fig. 28.5, a cross-clamped carotid during CEA is shown.

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Fig. 28.5  Case Example 1: Shown here is the carotid bifurcation during a CEA. The common carotid is to the right, and the internal and external carotids are on the left. The blue circles highlight the cross-clamps over each of the vessels

There are a few interesting occurrences in this case. The propofol bolus causes an increase in the amplitude of the SSEP due to the change in morphology or by improving signal to noise ratio by decreasing spontaneous EMG. The left median SSEP initially decreases in amplitude immediately upon cross-clamping but soon recovers. It may have also been warranted to proceed with a shunt at that point. This case also illustrates the potential added value of MEPs, as there was loss of the hand MEP before there was a critical change in the amplitude of the left median SSEP. Although we would expect that primary sensory and motor cortex would be equally affected by carotid clamping, the signals may not respond equally fast to ischemia, and having redundant coverage can increase the sensitivity. Motor evoked potentials do not have to be averaged, so a change can potentially be detected faster if those are run frequently. Additionally, if there was subcortical ischemia causing pure motor deficits, SSEPs would be insensitive to this. It should also be noted that as the patient was in burst suppression during cross-clamping, making it difficult to rely on the EEG for detecting ischemia, there is increased importance in the inclusion of the other modalities.

Case Example 2 A 67-year-old woman presented with recent worsening of chronic headaches and was diagnosed with a 4 mm left M1 MCA aneurysm with secondary subarachnoid hemorrhage. Physical exam showed no preoperative sensorimotor deficits. She underwent a left frontotemporal craniotomy for clipping of the aneurysm using IONM.  IONM was performed with upper and lower SSEPs, TcMEPs, and two channels of EEG.  Figures  28.6, 28.7, 28.8, and 28.9 summarize the relevant IONM events. After recovery of the TcMEP, the aneurysm was successfully clipped using two different clips, and there were no further IONM changes during the remainder of the case. The patient awoke with mild right arm weakness that resolved within minutes after being fully awake, and she had no other deficits during her hospitalization.

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Fig. 28.6  Case Example 2: The baseline SSEPs and EEG are shown

Fig. 28.7  Case Example 2: TcMEPs obtained 5  min after permanent clip application remain unchanged from baseline

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b

Fig. 28.8  Case Example 2: Loss of the right-hand TcMEP during dural closure, 23 min following clipping of the aneurysm, with no associated SSEP change

Case Example 3 A 64-year-old male was incidentally found to have 10 mm anterior communicating artery (ACOM) aneurysm while being staged for bladder cancer. Because of the size of the aneurysm and associated risk for hemorrhage, surgical clipping was recommended (Fig. 28.10, arrow). A left craniotomy for clipping of the aneurysm under mild hypothermia and IONM was performed. IONM was done using upper and lower SSEPs and TcMEPs and two channels of EEG. Figure 28.11 shows SSEPs obtained during the case. As indicated above each panel, the left-to-right panels show cortical SSEPs over a period of 90 min from left and right median and left and right posterior tibial nerve stimulation, respectively. Down arrows indicate baseline lower extremity (LE) SSEPs, and the right arrow points to loss of bilateral LE SSEPs, which occurred during temporary occlusion of bilateral A1 arteries and before placing the permanent clip. The surgeon was informed of the LE SSEP change, and the patient’s MAP was increased to >90 mm Hg. Major LE SSEP changes lasted approximately 25 min. During this time, the temporary clips were briefly removed on two occasions to provide vessel reperfusion. A permanent clip was successfully placed and complete SSEP recovery occurred 35 min after the initial change. The up arrow shows recovery to baseline levels of the LE SSEP.  Note that there are no changes in the upper extremity (UE) SSEPs.

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a

a b

c

Fig. 28.9  Case Example 2: The surgeon was notified of the change, the dura was reopened and the clip was removed. (a) Removal of the permanent clip resulted in the right-hand TcMEP returning to baseline levels (arrow). (b) Position of the permanent clip (arrow) prior to removal. (c) A small vessel (arrow) was noted behind the aneurysm, which likely became occluded during closure due to clip migration Fig. 28.10  Case Example 3: Computed tomography angiography with 3D reconstruction showing ACOM aneurysm (arrow)

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Fig. 28.11  Case Example 3: Cortical SSEPs from all four limbs

Fig. 28.12  Case Example 3: TcMEPs obtained during the period of temporary bilateral A1 artery occlusion

Figure 28.12 shows the TcMEPs obtained during the period of temporary bilateral A1 artery occlusion. TcMEPs were performed using threshold stimulation intensity levels required to elicit only contralateral LE TcMEPs to reduce the likelihood of activating deep subcortical corticospinal pathways. Note that each stimulation session activates TcMEPs only from one side, never from both. Down arrow points to the presence of left foot (AH) TcMEPs while the up arrow to those from the right foot. These did not change from baseline at any point during the case.

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This example demonstrates how cerebral ischemia can be bypassed or “undercut” in certain circumstances when using TcMEPs and why it is important to use multimodality monitoring with SSEPs and EEG. The patient did well and did not have any postoperative neurologic deficits.

Case Example 4 A 69-year-old female with history of hypertension and hypothyroidism who 4 months prior to presentation stopped taking her antihypertensive medications due to side effects. A day prior to admission, she felt dizzy, and her gait was unsteady. She rested but her symptoms persisted. She was taken to an outside hospital where a brain CT scan without contrast demonstrated 2  cm × 1.3  cm slightly irregular, global mass, ventral and slightly superior to the medulla, causing local mass effect. Further evaluation revealed a giant basilar artery aneurysm (Fig. 28.13). Neurologic exam was notable for moderate anxiety but was otherwise normal. In the ICU, the patient experienced an episode of acute faintness associated with bradycardia to the 30s and MAPs in the 40s. She subsequently rapidly recovered to her baseline. This was felt likely to be an effect of midbrain compression caused by the aneurysm. Due to the surgically inaccessible location of the aneurysm and the limited endovascular options, she was treated with a novel stent system and IONM.

Fig. 28.13  Case Example 4: Angiogram showing a 2.5 cm inferior basilar trunk aneurysm

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IONM was performed using UE and LE SSEPs and BAEPs. The surgeon requested the use of neuromuscular blocking agents during the case to avoid any movement due to the high risk for aneurysm rupture, so TcMEPs were not used. Figure 28.14 shows the baseline SSEPs and BAEPs. Panel A shows left median nerve SSEPs; top two traces are cortical scalp recordings; third trace is C7–Fz; fourth trace is Erb’s point–Fz. Panel B shows right median nerve SSEP, with similar montages as in A. Panels C and D are left and right posterior tibial nerve SSEPs, respectively. The top three traces are all cortical scalp recordings, Cz–Fz, Cz′–Fz, and C3′/C4′ contralateral; and the bottom trace is C7–Fz. Left BAEP montage is Cz–A1 and the right BAEP is Cz–A2. Figure 28.15 shows amplitude reduction of the right BAEP (arrow) after placement of the microcatheter in the right vertebral artery. This worsens several minutes later as shown in Fig. 28.16 by loss of the right BAEP (arrow). Note that there are no changes in the SEPs or the left BAEP. The surgeon was alerted after the initial BAEP amplitude reduction and the microcatheter was removed. Upon removal of the microcatheter, the right BAEP quickly recovered (Fig.  28.17, arrow). These changes occurred during the two periods, 6 and 11  min, respectively, when the microcatheter was in the right vertebral artery placing the stents. There were no further changes noted after the placement of three stents from her right vertebral artery into her basilar artery. Her left vertebral artery was then occluded using coils. She woke from the procedure without any neurologic deficits, and she was discharged 3 days later. Her postoperative day 6 CT angiography shows normal posterior circulation blood flow and minimal residual aneurysm (Fig. 28.18).

a

b

e

c

d

f

Fig. 28.14  Case Example 4: Baseline SSEPs and BAEPs. (a) Baseline left median nerve SSEP (b) Baseline right median nerve SSEP (c) Baseline left posterior tibial nerve SSEP (d) Baseline right posterior tibial nerve SSEP (e) Baseline left BAEP (f) Baseline right BAEP. The montages used for each evoked potential are further described in the corresponding section of the case description

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Fig. 28.15  Case Example 4: Reduction in the amplitude of the right BAEP following placement of the microcatheter in the right vertebral artery

Fig. 28.16  Case Example 4: Loss of the right BAEP following placement of the microcatheter in the right vertebral artery

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Fig. 28.17  Case Example 4: Recovery of the right BAEP within several minutes of removal of the microcatheter from the right vertebral artery

Fig. 28.18  Case Example 4: CT angiography of the head shows normal posterior circulation blood flow and minimal residual aneurysm post-procedurally

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somatosensory evoked potentials, transcranial Doppler, and near-infrared spectroscopy. Neurol Clin. 2006;24(4):631. 121. Steiger HJ, Schäffler L, Boll J, Liechti S. Results of microsurgical carotid endarterectomy – a prospective study with transcranial Doppler and EEG monitoring, and elective shunting. Acta Neurochir. 1989;100(1–2):31–8. 122. Sundt TM. The ischemic tolerance of neural tissue and the need for monitoring and selective shunting during carotid endarterectomy. Stroke. 1983;14(1):93. 123. Sundt TM, Sharbrough FW, Anderson RE, Michenfelder JD.  Cerebral blood flow measurements and electroencephalograms during carotid endarterectomy. J Neurosurg. 1974;41(3):310. 124. Sundt TM, Sharbrough F, Piepgras DG.  Correlation of cerebral blood flow and electroencephalographic changes during carotid endarterectomy with results of surgery and hemodynamics of cerebral ischemia. Mayo Clin Proc. 1981;56:533. 125. Symon L. The relationship between CBF, evoked potentials and the clinical features in cerebral ischaemia. Proc 23rd Scand Neurol Congr Acta Neurol Scand. 1980;62:175. 126. Symon L, Crockard HA, Dorsch NWC, Branston NM, Juhasz J. Local cerebral blood flow and vascular reactivity in a chronic stable stroke in baboons. Stroke. 1975;6(5):482. 127. Takamura Y, Motoyama Y, Takatani T, Takeshima Y, Matsuda R, Tamura K, et  al. Motor evoked potential monitoring can evaluate ischemic tolerance to carotid artery occlusion during surgery. J Clin Monit Comput. 2021;35(5):1055–62. 128. Tanabe J, Ishikawa T, Moroi J.  Safe time duration for temporary middle cerebral artery occlusion in aneurysm surgery based on motor-evoked potential monitoring. Surg Neurol Int. 2017;8(1):79. 129. Thiagarajan K, Cheng HL, Huang JE, Natarajan P, Crammond DJ, Balzer JR, et al. Is two really better than one? Examining the superiority of dual modality neurophysiological monitoring during carotid endarterectomy: a meta-analysis. World Neurosurg. 2015;84(6):1941–1949.e1. 130. Thirumala PD, Thiagarajan K, Gedela S, Crammond DJ, Balzer JR.  Diagnostic accuracy of EEG changes during carotid endarterectomy in predicting perioperative strokes. J Clin Neurosci, Churchill Livingstone. 2016;25:1–9. 131. Thirumala PD, Udesh R, Muralidharan A, Thiagarajan K, Crammond DJ, Chang YF, et al. Diagnostic value of somatosensory-evoked potential monitoring during cerebral aneurysm clipping: a systematic review. World Neurosurg. 2016;89:672–80. 132. Tiberio G, Floriani M, Giulini SM. Monitoring of somatosensory evoked potentials during carotid endarterectomy: relationship with different haemodynamic parameters and clinical outcome. Eur J Vasc Surg. 1991;5(6):647. 133. Trojaborg W, Boysen G. Relation between EEG, regional cerebral blood flow and internal carotid artery pressure during carotid endarterectomy. Electroencephalogr Clin Neurophysiol. 1973;34(1):61–9. 134. Udesh R, Natarajan P, Thiagarajan K, Wechsler LR, Crammond DJ, Balzer JR, et  al. Transcranial doppler monitoring in carotid endarterectomy: a systematic review and meta-­ analysis. J Ultrasound Med. 2017;36(3):621–30. 135. Wahr J, Tremper KK, Samra S, Delpy DT. Near-infrared spectroscopy: theory and applications. J Cardiothorac Vasc Anesth. 1996;10(3):406. 136. Wassmann H, Fischdick G, Jain KK. Cerebral protection during carotid endarterectomy–EEG monitoring as a guide to the use of intraluminal shunts. Acta Neurochir. 1984;71(1–2):99. 137. Whittemore AD.  Carotid endarterectomy and alternative approach. Arch Surg. 1980;115(8):940. 138. Wilent WB, Belyakina O, Korsgaard E, Tjoumakaris SI, Gooch MR, Jabbour P, et  al. Intraoperative vascular complications during 2278 cerebral endovascular procedures with multimodality IONM: relationship between signal change, complication, intervention and postoperative outcome. J Neurointerv Surg. 2021;13(4):378–82. 139. Wöber C, Zeitlhofer J, Asenbaum S.  Monitoring of median nerve somatosensory evoked potentials in carotid surgery. J Clin Neurophysiol. 1998;15(5):429.

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Chapter 29

Intraoperative Neurophysiologic Monitoring for Thoracic and Thoracoabdominal Aortic Procedures Felix W. Chang and Jaime R. López

Abbreviations ACP AH ASA BCR CMAP CPB CSF CT DHCA ECI EMG EP HCA IONM mA MAP MEP

Antegrade cerebral perfusion Abductor hallucis Anterior spinal artery Bulbocavernosus reflex Compound muscle action potential Cardiopulmonary bypass Cerebrospinal fluid Computed tomography Deep hypothermic circulatory arrest Electrocerebral inactivity Electromyography Evoked potential Hypothermic circulatory arrest Intraoperative neurophysiologic monitoring Milliamps Mean arterial pressure Motor evoked potential

F. W. Chang (*) Department of Neurology and Neurological Sciences, Stanford University, Stanford, CA, USA e-mail: [email protected] J. R. López Department of Neurology and Neurological Sciences, Stanford University, Stanford, CA, USA Department of Neurosurgery (Courtesy), Stanford University, Stanford, CA, USA © The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 S. M. Verst et al. (eds.), Intraoperative Monitoring, https://doi.org/10.1007/978-3-030-95730-8_29

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MRA NPV PPV PSA RCP SACP SCBF SCI SNAP SSEP TA TAAA TcMEP TEVAR

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Magnetic resonance angiography Negative predictive value Positive predictive value Posterior spinal artery Retrograde cerebral perfusion Selective antegrade cerebral perfusion Spinal cord blood flow Spinal cord injury Sensory nerve action potential Somatosensory evoked potential Tibialis anterior Thoracoabdominal aortic aneurysm Transcranial motor evoked potential Thoracic endovascular aortic repair

Introduction Spinal cord ischemia and infarction has been a well-recognized and feared complication of thoracic aortic and thoracoabdominal aortic surgery since its earliest days. Development of spinal cord infarction can lead to paraparesis or paraplegia, a devastating neurologic injury. In 1951, Lam and Aram reported one of the first known thoracic aortic repairs. In their report, this initial patient developed marked lower extremity weakness and neurogenic bladder postoperatively, with partial recovery at discharge. Historical rates of paraparesis and paraplegia have been reported at 16% [99]. Surgeries of the thoracic or thoracoabdominal aorta carry a high risk of spinal cord ischemia as it is necessary to temporarily or permanently interrupt the intercostal or segmental arteries which supply the spinal cord. Following interruption of these arteries, the spinal cord will have increased reliance on the collateral network supplied by other blood vessels not arising from the aorta, such as the vertebral artery or the hypogastric vascular network. If this collateral network is not sufficient, then spinal cord ischemia will occur. A variety of methods have been investigated and implemented over time that have lowered the rate of spinal cord injury. IONM, the use of intraoperative neurophysiologic testing to monitor the integrity of neural structures, has gained popularity since its introduction in the field. IONM techniques can accurately identify intraoperative spinal ischemia to help guide intraoperative and potentially postoperative management. The goals of this chapter are as follows: 1. Review the vascular anatomy of the spinal cord. 2. Describe the neurologic injury which can occur in procedures of the descending aorta. 3. Describe the neuroprotective measures that can be taken. 4. Review the evidence base for the various IONM modalities. 5. Illustrate the practical aspects of IONM with clinical cases.

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Vascular Anatomy of the Spinal Cord To understand and recognize intraoperative spinal cord ischemia, a detailed knowledge of the vascular anatomy of the spinal cord is required. There can be great variability in the exact vasculature between patients, which may explain why some patients are more susceptible to injury than others. The overall blood supply of the spinal cord can be described as a collateral network with many different inputs. The anterior two thirds of the spinal cord is usually supplied mainly by the anterior spinal artery (ASA), which runs longitudinally along the anterior surface of the spinal cord. The posterior third of the spinal cord is usually supplied by two posterior spinal arteries (PSAs), which run longitudinally along the posterior surface of the spinal cord and parallel to each other. The ASA and PSA give rise to penetrating sulcal arteries which feed the interior portions of the cord. Along the thoracic and lumbar regions, the spinal cord receives blood flow from segmental arteries. These arise in pairs from the descending aorta. In the thoracic region, these segmental arteries are known as posterior intercostal arteries. Above T3, multiple segmental arteries may arise from the aortic arch or costocervical trunk as the superior intercostal artery. Below T3, each pair usually supplies a single spinal segment, and there are typically nine of these pairs. In the lumbar region, the segmental arteries are known as lumbar segmental arteries, with usually four pairs [86]. There are extensive communications between the segmental arteries at each level. At some levels, the segmental arteries will give off branches, anterior and posterior radiculomedullary arteries (or radicular arteries), which supply the spinal cord (see Fig. 29.1). At the cervical level, the ASA usually arises at the foramen magnum and is formed from branches descending from the vertebral arteries. The ASA extends to the conus medullaris distally [86]. Anterior radiculomedullary arteries derived from the segmental arteries provide additional blood flow to the ASA as it travels caudally. Although named and often drawn as a single continuous artery, the ASA may be better thought of as a series of anastomotic vascular loops derived from Y-shaped feeding arteries. Between these larger arteries, many connections exist, creating a continuous network of vascular arcades [48]. See Fig. 29.2. The PSAs originate at the level of the foramen magnum and are usually supplied by branches from the vertebral or posterior inferior cerebellar arteries. As the PSA descends, it is reinforced by blood supply from the posterior radiculomedullary arteries, which arise from the segmental arteries at each level [86]. Similar to the ASA, the PSAs can be discontinuous and can potentially cross from one side to the other at different levels. The PSA can be thought of as a ladder-like longitudinal network [48]. Transverse and oblique branches from the ASA and PSA form anastomoses between the arteries, forming the pial plexus. The pial plexus does not provide much collateral flow between the ASA and PSA, especially in the thoracolumbar regions. Compared to the ASA, the PSA has lower vascular resistance, as the PSA has more connections between large vessels. Higher resistance, among

664 Fig. 29.1  Radiculomedullary (radicular) arteries are given off branches of the intercostal and lumbar segmental arteries every few spinal levels. These arteries reinforce the spinal cord blood flow at these levels. Watershed zones exist between radicular artery segments. The lower thoracic cord is more prone to ischemia as there is less collateral flow present and may be mainly dependent on the artery of Adamkiewicz (arteria radicularis magna). (Reprinted with permission from Cheung AT, López JR. Spinal Cord Ischemia Monitoring and Protection. Evidence-Based Pract Perioper Card Anesth Surg. 2021;323–43. Copyright 2021 Springer Nature Switzerland AG)

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Vertebral

Intercostal

Watershed area

Lumbar

Internal iliac

other reasons, means the ASA is relatively more susceptible to ischemia than the PSA [48]. Porcine studies have shown that there is a high dependence on epidural arcades to provide immediate backup flow during aortic occlusion [56]. As the blood supply of the spinal cord is a collateral network, it is logical to assume that increasing perfusion pressure by increasing mean arterial pressure and/or decreasing cerebrospinal fluid pressure can augment blood flow and reverse ischemia. As the ASA is often discontinuous, areas between two feeding arteries can be susceptible to ischemia. Watershed levels have been observed at T1, T5, and T8–T9 [17, 40, 41]. The largest thoracolumbar anterior radiculomedullary artery is the artery of Adamkiewicz or arteria radicularis magna. This arises between T8 and L2 in 75% of patients but can also range from T5 to L4 [12, 16, 49, 60]. The artery of Adamkiewicz is important, as there is minimal collateral blood supply to the cord in the region the artery of Adamkiewicz supplies. There are typically no other anterior radiculomedullary feeders that arise below the level of the artery of Adamkiewicz

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Posterior spinal arteries Anterior spinal artery

Posterior radicular arteries Anterior radicular artery

Dorsal branch of intercostal artery

Intercostal artery

Aorta

Fig. 29.2  A transverse section of the spinal cord shows the typical blood supply at a given spinal level. A pair of segmental (intercostal or lumbar) arteries is given off from the descending aorta. These give rise to the anterior and posterior radiculomedullary (radicular) arteries, which reinforce blood supply to the anterior spinal artery and posterior spinal arteries. (Reprinted with permission from Cheung AT, López JR. Spinal Cord Ischemia Monitoring and Protection. Evidence-Based Pract Perioper Card Anesth Surg. 2021;323–43. Copyright 2021 Springer Nature Switzerland AG)

[86]. The levels at which radiculomedullary arteries arise vary between patients. Embryologically, initially these occur at regular intervals at every thoracolumbar spinal level. As development continues however, these regress at irregular segments, explaining the variability between patients [113]. The vascular anatomy of the spinal cord is of importance in thoracic aortic and thoracoabdominal procedures, as they involve periods of clamping of the descending aorta and can involve sacrifice of the intercostal arteries.

 verview of Spinal Cord Ischemia and Stroke in Procedures O of the Descending Aorta Incidence In Svensson et al. [99], a retrospective study of 1509 patients and 1679 thoracoabdominal aortic aneurysm (TAAA) repairs between 1960 and 1991 at a single center and one of the largest single studies on outcomes in TAAA, the overall incidence of paraplegia or paraparesis was 16% (234 of 1509 patients). The incidence of stroke was 3% (39 of 1509 patients). In a more contemporary study, by Coselli et al. [20],

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the rate of paraplegia/paraparesis was lower, likely the result of many improvements in surgical techniques over time. The authors looked at 2286 TAAA repairs at a single institution between 1986 and 2007 and found an incidence of 6.3% of spinal cord injury (SCI), and 1.7% of stroke. Thoracic endovascular aortic repair (TEVAR) was first approved in the USA in 2005 following the GORE TAG trial [72]. It was initially thought that TEVAR may have been associated with a lower risk of spinal cord ischemia. Compared to open repair, the aorta is not cross-clamped during TEVAR, which avoids any reperfusion syndrome and causes less physiological disturbances. In the original GORE TAG trial, which enrolled patients with isolated descending thoracic aortic aneurysms, 3% (4 of 142) of patients developed paraplegia, and 4% (5 of 152) stroke [72]. In Buth et al. [13], paraplegia or paraparesis was seen in 2.5% (15 of 606) of patients, and stroke was observed in 3.1% (19 of 606) of patients. A prospective comparison of surgical and endovascular repair was performed by Greenberg et al. [42]. The authors evaluated 724 patients and found no statistically significant difference in the incidence of SCI between the open and endovascular repair (7.5% vs 4.3%, p = 0.08). Similar rates of injury were also noted between the two techniques across different extent repairs. Unfortunately, the stroke incidence was not reported. Although not certain, the lower incidence of SCI in earlier studies was likely due to populations with less extensive aneurysms being enrolled. In subsequent studies rates appeared similar in TEVAR. Ullery et al. [105] reported 2.8% (12 of 425) of patients with SCI, Scali et al. [88] reported an incidence of 9.2% (68 of 741), and Dias et al. [26] reported an incidence of SCI of 31%.

Risk Factors In Svensson et al. [99], several risk factors for SCI were identified in open TAAA repair, which included total aortic clamp time, the extent of aortic repair, presence of aortic rupture, age, history of renal dysfunction, and concurrent presence of a proximal aortic aneurysm. Crawford extent II patients (proximal descending aorta to below the renal arteries), which made up 29% of patients (442 of 1509), had the highest incidence of SCI, at 31.5%, and additionally had a stroke rate of 5%. Figure 29.3 illustrates the Crawford classification system for aneurysms. Compared to extent I aneurysms (proximal descending aorta to the upper abdominal aorta), extent II aneurysms had an odds ratio of 1.73 for injury. The odds ratio for spinal cord injury compared to extent I aneurysms was 0.33 in extent III (distal descending aorta to the abdominal aorta) and 0.18 in extent IV (abdominal aorta). To summarize, the risk of SCI in descending order is extent II, extent I, extent III, and extent IV, which corresponds to increases in the involvement of the thoracic aorta. Each additional minute of aortic clamp time was associated with an odds ratio of 1.02 for paraplegia/paraparesis. In Coselli et  al. [20], extent II repairs again showed the highest incidence of SCI at 6.3%, compared to 3.3% in extent I, 2.6% in extent III, and 1.4% in extent IV.

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Incidence of Spinal Cord Ischemia According to the Crawford Classification of Thoracoabdominal Aortic Aneurysm Extent

I Endovascular Repair Open Surgical REpair

10% 14%

II 19% 22%

III

IV

5% 10%

3% 2%

Fig. 29.3  The rates of spinal cord ischemia from Greenberg et al. [42] in endovascular and open surgical repair of TAAA are shown according to their Crawford class. (Reprinted with permission from Cheung AT, López JR. Spinal Cord Ischemia Monitoring and Protection. Evidence-Based Pract Perioper Card Anesth Surg. 2021;323–43. Copyright 2021 Springer Nature Switzerland AG)

The degree of repair in TEVAR was similarly found to be one of the main risk factors for developing SCI in Greenberg et al. [42], who compared endovascular and open surgical repair of TAAA. In extent II repair, where the highest rate of SCI occurred, the rate of SCI was 19% in endovascular repair and 22% in open repair. In TEVAR as well, multiple studies confirmed extent of repair/length of aortic graft as the main risk factor for spinal cord ischemia [9, 26, 88]. Some of the other risk factors that have also been identified include age, history of renal insufficiency, and duration of procedure [13, 88].

Timeframe SCI following TAAA repair can be seen in an immediate or delayed fashion. Most studies define immediate as occurring less than one day postoperatively. Delayed injury can occur after 1 day, or even several weeks later. In Greenberg et al. [42], which compared open and endovascular repair, most SCI tended to be delayed (more than 1 day postoperatively), 71% in the open repair group and 87% in the endovascular group. A similar trend was observed in Ullery et al. [105] where 83% of spinal cord injuries were delayed. Etz et al. [33] also observed in a series of 858 TAAA repairs that of the total of 20 patients (2.3%) who developed paraplegia, 3 of

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20 occurred intraoperatively, 10 of 20 occurred with 48  hours of surgery despite intact somatosensory evoked potentials (SSEPs) at the end of surgery, and 7 of 20 occurred later. Estrera et  al. [30] retrospectively analyzed factors that predicted delayed neurologic deficit in TAAA repair in 854 patients. The overall neurologic deficit rate was 6.9%, and the rate of delayed deficit was 2.7%. They found that preoperative renal dysfunction, acute dissection, and extent II repair were significant predictors of a delayed deficit. Additionally, the authors found that using adjuncts such as distal aortic perfusion and CSF drainage was associated with an increased risk of delayed ischemia (p  40 minutes had a stroke rate of 13.1% compared to 3.3% in cases